CHALLENGING BASIC ASSUMPTIONS:
A reassessment of marine nitrogen
flux patterns, including biological controls on the availability of nitrogen in
seawater. And finally, a MEDICAL DIAGNOSTIC MODEL for a STARVING OCEAN
It is hypothesized that a generalized ‘starvation’ is at the root of today’s
failing marine life, and that total marine production has been steadily lowered,
both developments representing an unintended, and unrecognized, consequence of
fishing. Prior scientific investigation into this hypothesis appears to be
lacking. Mainstream scientific thinking on the hypothesis, however, has been to
firmly resist the idea because of the belief that marine production is directly
linked to, and determined by, patterns of "physical forcing." (Berger et al,
1989, Carpenter and Capone, 1983, Parsons et al, 1984)
The physical forcing of dissolved nutrients from deeper waters to the sunlit
zone occurs as the result of seasonal weather patterns which are essentially a
constant. It was necessary therefore to demonstrate the point of disconnection
between physical forcing patterns and patterns of marine primary productivity.
This is best demonstrated by describing vertical nutrient flux patterns that
have not been accounted for, as such, in the literature. There are two features
of the biological system that actively counteract the sinking tendency of
organic material, one indisputable and the other hypothetical. The first is that
‘biological forcing’ of primary production is achieved to some extent in
continental shelf systems where assemblages of benthic invertebrates and fish
release prodigious numbers of floating pelagic spawn. Traditionally viewed only
as a "reproductive strategy" (Kasyanov, 2001, Steidinger and Walker, 1984), this
spawning behavior also represents an important, biologically forced, nutrient
flux that has not been quantified or considered in the standard ecosystem
models. Just as nitrates forced to the surface by weather patterns will
stimulate primary production, so will the physical raising of eggs and larvae.
The quality of the effect on phytoplankton productivity is the same. Secondly,
it can also reasonably be hypothesized that vertical migration patterns of
zooplankton may accomplish an upward shift of dissolved plant nutrients, since
these animals appear to have the ability to absorb dissolved food directly from
the water (Steidinger and Walker, 1984), and they undertake long daily vertical
migrations within the water column.
If biological forcing has therefore played an important role in all ocean
systems (and not only the tropical ones, where the idea was recognized decades
ago), then significant biomass removal by fishing has potentially lowered system
productivity. This potential, for net system productivity to have been lowered
as a consequence of fishing, has not been clearly recognized in recent
literature that has sought to discover the extent of the ecosystem effects of
fisheries. (Jackson et al, 2001, Kaiser and deGroot, 2000, Goni, 2000)
A model of an individual starving marine population (Powell et al., 1995) was
used to predict which symptoms might emerge on a more general scale if
‘starvation,’ or bottom-up control, were increasingly exerted on the ocean
itself. The model revealed the likelihood of only a single early warning signal,
loss of the older members of the affected population, which could easily be
misinterpreted as a sign of overfishing. Differential diagnosis at a systemic
level relies on finding the signal in unfished, as well as fished, populations.
In an attempt to find meaningful patterns in the larger picture of broad
changing trends in marine life today (the "down the web" shift, the failure of
Atlantic groundfish stocks to recover under moratorium, the widespread decline
in the age and size at maturity of fish, the increasing incidence of harmful
algae blooms, changes in seaweeds and intertidal invertebrates, the starvation
of marine mammals, etc…), I have drawn parallels between what appear to be
physiological homeostatic mechanisms at work in the overall ocean system and
similar biological processes that are known to act to maintain a smaller living
system - the human body. It was important to demonstrate that long-term
consistency in measurements of seawater nitrogen (usually nitrate) concentration
is unrelated to long-term changes that may have occurred in rates of primary
With a background in an older biological scientific discipline, the study of
human medicine, I have taken the approach of using a medical diagnostic model to
assess both the state of the ocean’s health today and also the value of the
currently favored diagnostic tests used by marine scientists. Many assessment
tests used today, especially those for "eutrophication," are unacceptably prone
to giving false positive results.
Signs of extreme stress due to nutrient loss emerge when the overall marine
ecosystem is assessed in this manner. And acute, and possibly abrupt, downward
shifts appear imminent as the biological system enters "decompensation."
1. IS THERE A USEFUL MODEL FOR STARVATION IN MARINE POPULATIONS OR ECOSYSTEMS?
Systemic nutrient depletion is postulated as a possible development in large
marine ecosystems if the bulk of nutrients removed in the form of fish has not
been effectively replaced. If, for some reason, fishing has caused an
interruption in nutrient cycling, systemic nutrient depletion might have
occurred. While there has be no evidence of active scientific suspicion on this
point, the possibility is presumably one that does exist. Or, systemic
starvation could conceivably result from a significant climate change, if ocean
currents were to change significantly. Regardless of cause, would we recognize
systemic starvation of the ocean if it occurred? Do we have the ability to
predict what a "starving ocean" or a population of "starving" marine organisms
would look like?
Attempts to develop multispecies models to predict the effects of perturbations
on aquatic systems have generally been so complex, with so many poorly
understood variables that they are unworkable. There are too many unknown
interactions, and even attempts to model populations of 2 or 3 species that
interact directly as predator and prey have not yet become highly reliable. Add
this to the lack of mainstream suspicion regarding biomass depletion as a cause
of decreased marine nutrient cycling, and no comprehensive models exist to
predict the changes that would be exhibited if a large marine ecosystem were
subjected to increasing degrees of bottom-up control.
My research turned up one potentially useful model however, one that predicts
the impact of declining food availability on the population dynamics of a single
Powell et al (1995) modeled oyster populations versus declining phytoplankton
stocks in Galveston Bay. The results of the model projections seemed to be
somewhat unanticipated by the researchers who developed it, since only one early
signal of starvation emerged from the population as a whole: This signal was
the disappearance of the larger individuals. This seems contrary to what we
might intuitively expect to see, which might be a slowed growth of all
population segments. But according to those authors:
"The simulations suggest that a reduction in market-size individuals is the
primary early-warning signal of decreased food supply within the affected
population and that this warning signal might easily be mistaken for overfishing.
Proper management requires the monitoring of food supply and the use of a
mathematical model to assess the importance of observed declines in population
abundance. Unfortunately, once the fishery is affected, little time may remain
before the termination of spawning and population extinction."
The numbers and the condition of juveniles and smaller reproductive adult
oysters remained steady, or even increased, under the onset of food limitation
of the population. This scenario persisted for a number of years before the
population underwent a relatively precipitous decline as reproduction failed.
Food loss selectively eliminated only the largest individuals first, and
initially had no noticeable effect on the population of smaller oysters. This
starvation model, about as simple as one can get, using a sessile plankton
feeder whose diet is unchanging throughout its life, was still a very complex
piece of mathematical work. The effects of multiple variables such as
temperature, turbidity, water flow rates and other factors that can impact on
the growth, fecundity and larval survival of oysters, all needed to be factored
in. An important conclusion of Powell et al. was that the onset of bottom-up
control could easily be confused with over fishing and that the immediate cause
of mortality in the larger individuals might appear to be over harvest or an
outbreak of disease.
It can be seen from the sequence of population changes in the model that the
maximum size obtained by individuals is related directly to the rate of primary
production in the system, since that is the single parameter that declined as
food availability decreased. Maximum size of individuals can therefore be used
as a proxy indicator of primary production. The relationship between the two
variables is not linear however, since a point is reached at which a further
small decline in primary production triggers a relatively abrupt extinction of
It is postulated that the basic principles revealed by the oyster v.
phytoplankton model will apply in a similar manner to an entire aquatic system
if basic production and food availability were gradually lowered. Mobile marine
species that feed on plankton for their whole lives, while more difficult to
model, would predictably show a similar pattern if a decline in plankton
availability were to occur in their environment. Broad changes across multiple
species within the larger ecosystem would also presumably be essentially
consistent with the principles revealed by the model.
It is very important to take note of how the subtle switch between top-down and
bottom-up control of populations will not be accompanied by any specific warning
signal that will be detected in the standard stock assessment approach.
Powell et al. emphasize two points in the discussion of their model. The first
is that a decline in the abundance of larger individuals is the one and only
signal of increasing bottom-up control that will be revealed in population
dynamics. Their second point emphasizes the importance of monitoring of the base
of the food chain when scientists are gathering relevant information to be
considered in fishery management.
Powell et al’s description of the effects of a declining food supply on the
oyster population illustrates just how difficult it can be to detect this cause
of population decline and to distinguish it from overfishing. They paint a
picture of a population of normal looking oysters, growing, reproducing and
showing condition factors within normal. All that changes is that the high end
of the population gradually crumbles away, as only the oldest individuals weaken
and die from starvation. That is how the dominos fall.
A stock assessment approach that detailed the growth and condition parameters
for each age-cohort separately might be expected to demonstrate the selective
decline in the health and condition of the largest ones, but any approach that
merely averaged growth rates and condition factors for whole populations might
not reveal any significant changing trend during the onset of food limitation in
It bears mention at this point that some intensively monitored fish stocks do
have time-series data on growth indices in individual age cohorts. One of these
is the infamous Northern cod stock on the Grand Bank of Newfoundland in Atlantic
Canada. A decade ago this stock experienced a precipitous population crash and
the remnant population, although under a fishing moratorium, continues to
decline. The hypothesis that shifting climate variables were responsible for the
crash has been convincingly disproved. (Myers and Hutchings, 1994) The stock
assessments on the Northern cod clearly do indicate a trend of declining growth
in each of the older age cohorts before they disappeared from the data tables.
(Lilly et al, 1999, see especially Fig. 16) And the same assessments revealed
the basically unchanging health of the youngest cod under whatever
"environmental conditions" forced the crash of the older fish. This is very
consistent with the predicted changing patterns that are suggested by the
population starvation model.
Powell et al’s model of the increasingly food-limited oyster population
demonstrates that the isolated effect is simply a contraction of the scope for
growth of individual oysters in the environment. Considered across entire marine
populations, a reduction in the scope for growth might also be expected to
translate into a contraction of the extent of the range occupied. The outer
limits of the ranges of organisms curtail their growth due to some aspect of the
physical environment that becomes incompatible with physiological capacity of
the organism to cope with it. It may follow therefore that the onset of
generalized food-limitation might cause a quicker collapse in these already
marginal sectors of the population.
Examples consistent with this suggested pattern of range contraction can also be
easily found in today’s changing fish populations. Consider the American
lobster, a commercially valuable crustacean, ranging historically from
Newfoundland to Long Island Sound. Both the northernmost and the southernmost
populations of the American lobster have declined in recent years. The decline
of the Newfoundland lobster fishery has received relatively little attention,
but has in fact occurred. (DFO, 1998) The sudden crash of the southernmost
segment of the lobster population in Long Island Sound, however, has attracted a
considerable amount of public, media and scientific attention. Three years
later, no clear cause for this population collapse has been determined. Shell
disease is increasingly a plague affecting the lobster in the southern parts of
the New England fishery, and a decline in catch rates is also beginning to be
noticed in those areas. In the middle of the American lobster’s range, however,
centered on the Gulf of Maine and the Bay of Fundy, phenomenal catches of
lobster are still being made. While tonnage landed has remained very high,
concern has been expressed in recent years about the noticeable decline in the
average size of lobsters caught. And a recent change in the Nova Scotian fishery
also seems to be a warning sign: lobsters caught in the "offshore" or "midshore"
grounds are now in much poorer condition that those caught nearer to the coast.
Low meat weights, low protein content, and high mortality rates in the lobster
holding facilities have recently devalued the offshore segment of the Nova
Scotia lobster catch. (Personal communication from commercial fishermen directly
involved in this fishery.) This may indicate the onset of a contraction in the
offshore extent of the lobster’s range, and the signs of food limitation are
rather obvious in this case.
Observations like these two, regarding the changes in the populations of
Northern cod and American lobster, and their consistency with the model of
starving oyster populations…these changes should give us pause to think. And to
seriously consider the (disastrous) possibility that starvation is increasingly
lowering the ceiling for growth of all marine life. The two "sudden crash"
stories, of Newfoundland cod and Long Island Sound lobster, these should serve
as warnings to us of what may potentially occur on a much wider scale.
Fished populations have their age structures artificially lowered by the
fishing. Therefore, a lowering of the ‘ceiling,’ or their potential for maximum
growth in the ecosystem would go unnoticed if only the fished species were
observed. ("Carrying capacity" is a related concept to this idea of a ‘ceiling’
although carrying capacity focuses more on abundance and total biomass rather
than zeroing in on the maximum age attainable by individuals in the
environment.) When the ‘ceiling’ is lowered to meet the age at which the fishery
has been harvesting the fish, a sudden population crash occurs which appears to
be out of proportion to the level of immediate fishing exploitation.
The "crash" will seem to have been triggered by an "environmental" factor, which
in fact it has been. The perception in these cases has then been that if the
cause is "environmental," that then the cause is not "fishing." Seemingly never
considered in the standard interpretations is how centuries of fishing has
completely altered and diminished the entire character of the marine ecosystem.
It looks now as if one effect may have been a gradual, constant erosion of the
total marine productivity, with a resultant ‘lowering of the ceiling for growth’
on virtually everything in the sea.
If marine nutrient cycling rates have been diminished by fishing, how exactly
might this have occurred? Analysis of the question requires a re-evaluation of
long-held assumptions about marine nutrient cycling. The approach I have taken
to this, in the next section of this report, is to draw an analogy between
biological homeostatic mechanisms that control the composition of blood and
those that maintain the composition of seawater.
2.BIO-AVAILABLE NITROGEN WITHIN THE PHOTIC ZONE OF THE OCEAN AND MAMMALIAN BLOOD
GLUCOSE: FUNCTIONAL ANALOGS IN BIOLOGICAL SYSTEMS?
Many signs today indicate poor growth in multiple marine organisms, which seems
to suggest declining total productivity, yet stable levels of bio-available
nitrogen in seawater appear to negate the possibility of a systemic nutrient
shortage. Is this a valid conclusion?
A fundamental similarity between human blood and seawater has been noted for
some time. The ratio of concentrations of the major ions is identical in both
liquids, for instance. Basic features of seawater and blood, primal
life-supporting fluids, appear to be essential to the sustenance of living
cells, organisms, and perhaps even systems.
In an attempt to illustrate why levels of bio-available nitrogen (hereinafter
nitrogen) in seawater would not be expected to drop in initial response to
systemic nutrient depletion, an analogy is drawn between nitrogen in marine
biological systems and blood glucose in mammalian biological systems (e.g.
Seawater nitrogen and blood glucose are analogous compounds in their
significance and the functional roles assumed in the ‘ocean organism/system’ and
the ‘human organism/system’ respectively. The essence of the difference reflects
only the difference between autotrophic (e.g. the ocean as a single entity) and
heterotrophic (e.g. human) organisms. Functional design principles are
essentially the same in many living systems. And that is where the similarity
between blood glucose and ocean nitrogen lies. Growth of the marine autotroph is
essentially protein limited, while growth of the heterotroph is basically carbon
limited…hence the similarity of the roles played by ocean nitrogen and blood
glucose. Although chemical differences between the two compounds obviously
exist, it is the functional roles played by blood glucose and ocean nitrogen as
the basic drivers/controllers of metabolic processes in their respective systems
that are highly similar.
In each case, the ‘ocean organism’ and the ‘human organism,’ the compounds in
question function simultaneously as critical building blocks and as crucial
elements in the processes involved in ‘harnessing energy’ or carbon intake and
accumulation by the organism. The supply of the key compounds, nitrogen and
glucose, determines how much energy, or fixed carbon, is taken in and stored by
their respective organisms. And the continued life of both ‘organisms’ depends
on the continued availability of these crucial materials. Nitrogen and glucose
also must be present in solution in water, and maintained within the tight range
of concentration values that is conducive to supporting the continued biological
processes of the living systems or ‘organisms.’
Therefore, to maintain optimal functioning, each of these biological systems has
evolved with intricate control systems and feedback mechanisms that work to
stabilize the availability of the key compounds. And a very high physiological
priority has been placed on maintaining ocean nitrogen and blood glucose within
normal levels (of both supply and concentration) - in fact, in both cases these
will be biologically stabilized by the living system literally "at all costs."
In the human example, the complex of physiological mechanisms that act in
concert to maintain stable blood glucose levels are now fairly well understood
by students of human medicine (although doubtless the complete complexity of the
system has yet to be described). Body systems directly involved in maintaining a
stable supply and concentration of blood glucose include the digestive,
circulatory, endocrine, renal, hepatic and lipid storage systems (fat).
Should the blood glucose level rise too high ("hyperglycemia"), immediate
physiological reactions occur that tend to lower it. This includes an
acceleration in the production of insulin, which hastens the absorption of
glucose into somatic cells, along with the prompt excretion of glucose through
the urine. On the other hand, if the concentration of blood glucose drops too
low ("hypoglycemia"), besides the development of hunger, hormonal processes act
to stimulate the release of stored glucose, both from more the quickly
accessible short-term storage depot (glycogen) and from the the body’s more
long-term energy storage depot (body fat).
Biological processes analogous to these also function in the ocean to ensure
stability of the supply and concentration of nitrogen in seawater. Briefly (and
explored in more detail in the next section of this report), the ocean-system
processes that act to compensate for low nitrogen in the photic zone are
nitrogen fixation by cyanobacteria, the production of pelagic spawn by many
organisms, possibly the vertical migration behavior of zooplankton, and various
strategies designed to remobilize nitrogen that is being held in temporary
storage depots. The ‘storage depots’ for nitrogen in the sea are living
organisms, therefore ‘remobilization’ strategies necessarily include the killing
of higher animals…starvation, plus the production of toxins specifically
designed to kill these creatures, are the processes that accomplish this end.
Interestingly…it can be seen that the lower, smaller creatures, such as the
legions of small marine invertebrates, are not vulnerable to the marine
biotoxins. Why not? This seems most likely to be because of their major role as
stabilizers of the zooplankton (which is analogous to the vital cellular
component of human blood). And how do invertebrates stabilize zooplankton? By
the production of prodigious numbers of floating spawn, marine bivalves,
crustaceans, echinoderms and others are major contributors to the zooplankton,
and thereby also to the stability of nitrogen availability in the photic zone.
This class of marine organisms can therefore be perceived to be roughly as
important to the ocean as bone marrow is to the human (…and bone marrow will not
be liquidated to maintain basic metabolism until the very last stage of the
Spawn production by benthic invertebrates is virtually equivalent to straight
‘zooplankton production’ due to the high mortality rates normally experienced by
the pelagic young of all spawning species. Invertebrates do not produce all of
the marine spawn in the ocean, however. Fairly high numbers of spawn are also
produced by the majority of bony fishes.…and one role that they play in the
systemic effort to compensate for lowered nitrogen availability, appears to be
an increase in the priority placed on spawn production by these fish. Today we
see a widespread trend of declining age and size at maturity in marine fish, as
the ocean increases her efforts to stabilize the composition of her ‘blood,’
which is the seawater of the photic zone. Roe is forming in much smaller fish
now than was ever observed by biologists in the past. (Godo and Haug, Lilly et
al, 1999, DFO, 2000a) Greater numbers of floating eggs and pelagic larvae have
the effect of increasing the nitrogen supply in upper regions of the water
column. Therefore, the decrease in age and size at maturity of fish can
plausibly be hypothesized to be a compensatory reaction of the ‘ocean organism’
to a declining availability of nitrogen
The timing of spawn production is also noteworthy. Spawning, when all species
are considered, covers the entire year but occurs at a very high rate during
spring, summer and fall. This timing helps the ocean system to maximize the
opportunity for photosynthesis when light availability is greatest, and also
helps to ward off severe nutrient depletion of surface waters in summer.
As with the example of blood glucose, the other important aspect in the
maintenance of ocean nitrogen levels is having strategies in place for the
avoidance of nitrogen concentrations that are too high. Examples of this
process, the method by which the ocean lowers the nitrogen level, are easily
observed today in sewage polluted estuaries. Termed "eutrophication," the
sequence of events includes a heavy bloom of phytoplankton, which acts to absorb
the nitrogen from the water, followed by the sinking of the dead algae to the
bottom, where bacterial decomposition takes place. Oxygen is consumed by the
decomposition process, which then may induce the development of a degree of
hypoxia in bottom water. Low oxygen concentrations act to accelerate the action
of denitrifying bacteria, which work to rid the system of the excess nitrogen by
converting it back to the atmospheric form, gaseous N2.
In the ocean, therefore, the problem of excess seawater nitrogen is handled
quite effectively on a local scale, as compensatory mechanisms return the values
to normal. There are very localized coastal areas where this compensatory
mechanism for high seawater nitrogen has been overwhelmed by the constant high
input (anthropogenic runoff) and nitrogen levels in the water remain high, but
in the vast majority of marine areas seawater nitrogen levels are effectively
held the within normal range for ocean health.
There appears to be a lot more evidence today that the ocean is relying heavily
on her ‘nitrogen raising’ strategies rather than on her ‘nitrogen lowering’
Viewing the marine ecosystem in this manner may help to provide a clearer
insight into the relationship between the concentration of nitrogen in seawater
and total marine productivity. There is no expected relationship, since the
maintenance of stable nitrogen levels will be done by the living system "at all
costs." Just as measurements of blood glucose in humans reveals no information
regarding how much energy is being expended, nor whether the person is gaining
or losing weight, measurements of seawater nitrogen concentrations are of no use
in estimating rates of marine primary productivity, or of the magnitude or
direction of the net flow of organic nitrogen.
An assumption of a constant rate of marine carbon flux (as has been made) simply
cannot be based on the observation of constant nitrogen levels in seawater. And
this same argument (with a few more twists) can be applied to the utility for
this purpose of measurements of chlorophyll concentration.
Unfortunately for those trying to gauge the health of the ocean, measurements of
nitrate and chlorophyll concentrations in seawater are essentially all of the
"nutrient"-related data that they have, that extends over any significant length
of time. (There exists about four decades of this data from various area in the
North Atlantic, for example, which reveals a general stability in nitrate levels
over that term. (e.g. DFO, 2001)) In recent decades marine scientists have come
to appreciate the limitations of this data and have devised methods for
recording the actual rate of carbon-uptake by phytoplankton. Many areas of the
world ocean have been sampled and measurements have been obtained of "grams of
carbon fixed per cubic (or square) meter per day." This provides ‘snapshots’ of
the primary productivity of different areas, but this data - although
laboriously obtained - also has limited usefulness for the purpose of my
particular inquiry: determining whether or not centuries of fishing has already
lowered the rate of marine productivity. One weakness in this approach is the
short time-span over which the rate measurements are taken - it is generally
about one day.
The other essential thing is to collect time-series data on primary production.
A program to do that has lately been part of an international effort by
scientists to monitor the health of the marine ecosystem (GLOBEC). Beginning in
1988, repeated measurements of primary production rates have been obtained at
two stations, one at Bermuda and the other in Hawaii. These are generating the
first time-series of data on phytoplankton primary productivity. The trends
revealed to date are of interannual fluctuations but no clear trend has emerged
yet. (Bates, 2001) One weakness in the method used (C14 uptake) is that carbon
taken up by cyanobacteria (N-fixers) is not distinguished from that taken up by
algae, so that the relationship between nitrogen cycling patterns and
productivity is difficult to determine.
The carbon flux of an organism can be estimated by a variety of other
observations, however, and this applies equally to the human and the ocean
systems. For a human, although it’s not a completely straightforward
relationship, carbon balance can be approximated by the quantity of body fat
that has accumulated. Fat is the primary organ that functions as a carbon depot.
(Factors such as environmental temperature, metabolic rate and activity level
have an impact on the amount of stored body fat, but a basic principle is well
known: individuals taking in larger amounts of carbon (food) will have
significantly greater fat stores than those who eat less.)
A look at which parts of the ocean system constitute the ‘fat,’ and trends over
time in this particular component of the ecosystem, will reveal important
information about long-term trends in marine primary productivity. (In the ocean
system, a functional autotroph, nitrogen storage will be roughly analogous to
carbon storage in the heterotrophic human.)
The remainder of this report will examine various aspects of marine ecological
processes from the standpoint of their roles in maintaining the stability of
nitrogen availability in seawater. Parallels between functional parts of the
living marine system and the roles played by different human body systems in
glucose metabolism, suggest an alternate view of how changes in the marine
ecosystem may be interpreted in the assessment of the overall "health" of the
ocean. This also suggests a means to estimate trends in marine carbon flux over
a longer term - whether the ocean has been maintaining a constant productivity
or alternately has been "losing weight." Physiological changes in a starving
organism are compared to today’s broad changing trends in marine life to gain
insight into whether or not "the ocean is starving."
3. MAINTENANCE OF "HOMEOSTASIS" IN THE SEA: BIOLOGICAL CONTROLS OF NITROGEN
AVAILABILITY IN THE PHOTIC ZONE
A system of complementary control mechanisms exists, along with feedback
patterns that switch these off and on as needed, the net effect of which is the
maintenance of optimal nitrogen availability in seawater to sustain continued
production of marine life.
(1) Biological processes that act to lower seawater nitrogen levels.
These are analogous to the ordinary metabolic processes that consume glucose and
prevent the accumulation of excess concentration of this chemical in human
First, it is obvious that the growth of phytoplankton involves the uptake of
nitrogen from seawater for use in the growth of the plant. This has an effect of
lowering the nitrogen concentration, and is analogous to the constant
consumption of blood sugar by the ordinary cell processes of living human
metabolism. There is no significant negative feedback working at this point:
available nitrogen in the photic zone will simply be taken up by the metabolism
of phytoplankton, in the same way that glucose, once it is within somatic cells,
will be completely metabolized. On that scale, the reaction only moves in the
one direction. An important point regarding nitrogen in the sea is that ammonia
(constantly excreted through the gills of all fish and zooplankton) is taken up
by phytoplankton much more efficiently than are other nitrogenous forms, such as
nitrate. (Lobban and Harrison, 1994) Therefore, ammonia will not accumulate to
any extent in surface waters due to the rapidity of uptake, and the quantity of
N-cycling mediated in this way can not be accurately determined with any type of
The second process that acts in the ocean to lower nitrogen in the photic zone
can be summed up as the ultimate tendency for organic particles to sink in
seawater. Dissolved nitrogen itself has no sinking tendency, but as soon as it
is incorporated into the forms of tiny algae (or bacteria) or things larger, the
tendency towards sinking becomes a major force. Growing by photosynthesis,
phytoplankton accumulate mass and may sink as a result, or they are consumed by
zooplankton, who, besides excreting the ideal N-fertilizer for phytoplankton
(ammonia) which stimulates more growth, also excrete sinking fecal pellets.
Bacteria grow in clumps on particles of detritus which also sinks. The net
effect of this is a "rain" of organic matter that constantly falls from the
photic zone to the seabed. The effect of this sinking tendency on nutrient
cycling is relatively well understood and described in the marine biology
A third process that acts to lower the concentration of nitrogen in seawater is
denitrification. Denitrification has the opposite effect of nitrogen fixation,
and is ordinarily not a major feature of marine nutrient cycling - it’s a
process that is triggered only when the nitrogen concentration becomes too high
(in waters affected by eutrophication, and to some extent in the seabed).
Denitrification is analogous to an excretory function that is used only when
needed; in the human analogy the comparable process is the excretion of sugar in
the urine. When the system is functioning in normal health, insignificant
amounts of sugar are excreted in urine, but when hyperglycemia develops,
excretion of sugar in the urine begins immediately and can reach high
proportions as the body seeks to maintain stability of the immediate
concentration of dissolved sugar in the blood.
(2) What forces act to complement the nitrogen-lowering processes, how does the
ocean system manage to replenish nitrogen in the surface water?
For nutrient cycling to be continuous in the ocean, there must be equivalent
physical forces that counteract the constant sinking tendency of organic matter.
Which forces are involved in refreshing the nitrogen supply in the surface
The best understood method by which nitrogen is returned to the surface water is
through forces that lead to physical mixing of the water column. This is not a
biological process, but the living system has evolved to co-ordinate its efforts
to use this natural phenomenon to full advantage. Seasonal cooling of the
surface in temperate zones as well as wave action, mix the richer bottom layers
with the upper, refreshing the potential for photosynthesis in the surface layer
through nitrate fertilization. Driven solely by annual weather patterns, this is
termed "physical forcing" and scientific recognition of this process has led to
a perception that weather patterns alone determine the rate of biological
production in the ocean. There is a vast reservoir of unavailable nitrate in the
deep ocean and on average, if weather patterns are constant, it stands to reason
that the same amount of this will be forced into the photic zone each year. If
the physical water movements resulting from weather patterns actually do control
the availability of nitrogen (as nitrate) in the photic zone, then the
assumption of a steady rate of marine carbon fixation (as long as weather
patterns are reasonably constant) is reasonable.
There are, however, biological processes that actively work to return nitrogen
to the surface waters, including processes that directly counteracting
sinking, and these processes also therefore affect the total rate of primary
productivity that occurs. In a more robust biological system these effects will
predictably be stronger, leading to the conclusion that the absolute rate of
marine carbon fixation is linked not only to "physical forcing" but also to the
number of functioning animate marine life forms in the sea.
First, it is worth noting, and has long been included in marine literature, that
the consumers of phytoplankton, the zooplankton, cycle nitrogen repeatedly
through the phytoplankton and thereby stimulate a greater level of net primary
productivity than what would occur in their absence. (e.g. Kerfoot and Sih,
1987) While this does not initially appear to entail an effect to
counteract sinking, it is the first biological function that acts to enhance
primary production. Since zooplankton growth, termed "secondary production," has
been envisaged as resulting as a direct consequence of "primary production,"
this fertilizing effect of the zooplankton has been also assumed to be, at its
basis, also "physically forced." This finding of cycling mediated by zooplankton
apparently has not changed the basic view that net system productivity is
physically forced because the cycling involved has been observed to occur within
the photic zone.
However a few facts about zooplankton would seem to complicate the
picture, and suggest that zooplankton may be involved directly in "biological
forcing" of production. The first observation is the fact that zooplankton do
not stay in the photic zone. They are well known to undertake long, daily
vertical migrations into the deeper, darker parts of the water column. Tiny
individual organisms may sink 50 meters or more during the day and then swim
back up to the surface waters each night. The exact reasons for this behavior
pattern remain a source of debate among scientists. (Steidinger and Walker,
1984) The vertical migration behavior appears to be energetically wasteful. But
another detail of zooplankton physiology may offer a clue as to one unsuspected
reason that might underlie the migratory behavior. Some zooplankton species,
notably the highly abundant copepods, appear to have the ability to uptake
dissolved organic material directly from the water. (Steidinger and Walker,
1984) Besides moving between high-light to low-light parts of the water column,
zooplankton are also moving between areas of lower and higher concentration of
dissolved nutrients during their daily migrations. This raises the intriguing
hypothesis that they may absorb nutrients directly from the deeper water and
raise those nutrients to the surface, where they may then be released to amplify
the fertilization of the phytoplankton. Zooplankton may also feed on detritus in
the deeper water and raise nutrients to the surface as a result of that
activity. Zooplankton might be visualized as a horde of little 'worker bees'
that continually pull organic nutrients from the depths toward the surface of
the sea...a part of the overall pattern designed specifically to counteract the
sinking of organic particles. In summary therefore, nutrient cycling mediated
by zooplankton cannot be considered to be purely a process that occurs within
the photic zone, and is therefore "physically forced"...because the zooplankton
do not physically stay at the top of the water column.
If the vertical migratory behavior of zooplankton accomplishes a net shift of
nitrogen, for instance, from lower to higher levels in the water column, it also
bears consideration whether or not this may also be a feature of similar
migratory behavior by some larger species, such as shrimp.
Notably absent from current analyses of marine ecological processes is an
appreciation of one major biological process that unarguably does act to
counteract the physical sinking tendency of organic matter and actively
regenerates bioavailable nitrogen in the photic zone from the seabed.
This process is the production of pelagic eggs and spawn.
Most marine spawn floats, and eggs and larvae released below the lower limits of
the photic zone can commonly be seen to float up into it. Important organisms
involved in this process include the bottom dwelling fish, but the greatest
contributors are the benthic invertebrates. This biological function, spawning,
actively transports N-rich organic material from the lower water column back up
into the photic zone.
Benthic organisms that feed low in the food web, capitalizing on sunken
phytoplankton or other detritus, play a major role in forcing the return of
organic nitrogen to the surface waters through the release of their floating
spawn. Many species, including bivalves and echinoderms, can be perceived as
devices that function to take in sunken phytoplankton and detritus and pump out
floating zooplankton. Individual organisms commonly release millions of gametes.
(Kasyanov, 2001) This is a slightly indirect, but very real, route by which
phytoplankton growth stimulates the production of zooplankton, and does not fit
the classic concept of the "secondary production" pathway because there is an
essential ‘middle man’ in the picture, in the form of the mature benthic
spawning organism. This is a quicker and more direct route by which nitrogen is
returned to the photic zone, than is the classic picture of sinking organic
material undergoing bacterial decomposition with the release of dissolved
nitrate into the bottom of the water column, eventually to be returned to the
surface by "physical forcing" triggered by weather patterns.
How does the pelagic spawn of benthic organisms act to replenish nitrogen in
First, by virtue of their normal metabolic processes as already discussed, even
if they consume nothing, all of these tiny organisms are ‘slow release’ devices
for ammonia. Secondly, even though they are only temporarily resident in the
zooplankton, many will engage in feeding on phytoplankton and recycling nitrogen
in place, contributing to the stimulation of greater levels of primary
productivity. Thirdly, these tiny eggs and larvae are frequently consumed by the
major species that constitute the full-time zooplankton, such as copepods and
chaetognaths, enhancing their growth and fertility, all of which enhances the
net rate of primary production by the phytoplankton. The pelagic spawn of
non-pelagic adults, when considered in total, makes up a very significant
fraction (sometimes the major fraction) of the total marine zooplankton biomass
in neritic waters. (Zhong et al, 1989)
"Secondary production" (aka "zooplankton production") is therefore clearly not
only linked to nitrate-driven primary production, but also to the size of the
total standing stock of pelagic spawn producers.
Humans have tended to view the development of the adult stage of these species
as the "goal" of their spawn production. This is merely a human bias, however,
perhaps colored partly by our desire to eat the adults produced, and also by our
perception that the goal of "reproductive strategies" of animals must be
analogous to ours, i.e. the survival of a maximum number of offspring to
maturity. But overwhelmingly, these invertebrates and fish "fail" to produce
more than miniscule "survival" percentages in their offspring, as the large
majority die during the pelagic life stages. This then, must be the primary goal
of the spawning behavior, effectively the production of zooplankton and the
physical raising of nitrogen-rich organic material from the seabed back up into
the photic zone.
The production of pelagic spawn by marine organisms, fish and invertebrates
both, therefore constitutes a ‘biological upwelling’ of nutrients in the coastal
ocean, which effectively enhances "secondary" production as well as "primary"
production. This appears to be one part of the intricately woven web of sea life
that was designed to counteract the tendency of organic particles to sink in a
liquid medium, a necessity in a growing medium where the sun shines only on the
Mother Ocean, you see, has long known how to deal with the gravity of the
Practically all marine species of fish and invertebrates will be classified as
zooplankton at some point in their lives. And when they do, they all occupy the
same "ecological niche" and perform the same "ecological role." The role played
at that stage is providing food for plankton-feeders as well as stimulating an
acceleration of primary production. For many marine species it is essential that
zooplankton be available for consumption, at least during the early life stages.
Phytoplankton alone will sustain very few of them. A very high priority is
therefore placed on the maintenance of a steady supply of zooplankton in the
The importance of zooplankton in ‘living’ seawater can be seen to be roughly
equivalent to the importance of the tiny blood cells that float in the liquid
medium on which human life depends. As with the concentration of nitrogen or
glucose, the next order of importance in maintaining healthy ‘lifeblood’ is the
concentration of the tiny individual blood cells or the tiny animal forms in the
sea, the zooplankton. Producers of pelagic spawn therefore, especially the top
producing invertebrates, many bivalves and echinoderms, are of a more critical
importance in maintaining ecosystem stability than are species groups that play
less central roles in this aspect of nutrient cycling. Like the bone marrow,
which produces our primary blood cells, these lowly invertebrates will be
maintained for a longer time under systemic starvation than will organisms whose
roles are more analogous to our body fat. Therefore, when the ecosystem is
forced to downsize and shift a greater fraction of its reserves into the
maintenance of the essential constituents of its ‘lifeblood,’ invertebrates such
as these will initially be spared.
How does the ocean mobilize its nitrogen reserves when this becomes a necessity?
Analogous to a starving person remobilizing stored energy reserves, some of the
tissue that performed the storage role will be broken down and the constituent
organic material shifted to places where it can be re-used to replenish the
essential ‘blood components,’ dissolved nitrogen and zooplankton. A shift in the
metabolic pattern occurs…the human may reverse the net process, going from
gaining weight to losing weight, but the internal metabolism will adjust
automatically to constantly maintain healthy blood. There appears to be two
major biological functions in the sea which act to remobilize stored nitrogen
for use in seawater maintenance. These are the production of biotoxins and
The production of biotoxins by marine phytoplankton appears rather inexplicable
to us at first glance, but a look at some of the details makes a plausible
argument that the production of these biotoxins is a system response to the
general lowering of the availability of dissolved nutrients, bio-available
nitrogen as well as phosphorus.
Biotoxins are produced by a variety of photosynthetic organisms across all major
groups of these - diatoms, dinoflagellates, cyanobacteria, members of all these
groups have been known to produce biotoxins under the ‘right’ conditions. (Lassus
et al, 1995) The most troublesome of these tend to be cyanobacteria and
dinoflagellates, and their toxicity to humans along with their increasing
prevalence in the world ocean, have drawn a fair amount of scientific attention
to the subject. The organisms that produce the biotoxins are typically smaller
than other types of phytoplankton, and are consistently known to bloom under
weather conditions that promote extreme levels of nutrient depletion in surface
waters (warm, calm spells: this type of weather very consistently precedes
blooms of toxin-producing phytoplankton, whether near shore or offshore,
dinoflagellates or cyanobacteria. (Lassus et al, 1995)) These types of plankton
can be difficult to culture in laboratory conditions, the cyanobacteria in
particular will grow only in extremely N-depleted media. This seems to be the
necessary condition to get the growth started, and when nitrogen levels start to
rise, cyanobacterial growth is inhibited. (Lassus et al, 1995) Cyanobacteria are
the only class of marine algae that can accomplish N-fixation and, probably for
this reason, they have long been known to be more prominent in oligotrophic
An interesting detail of toxic cyanobacterial culture is that the concentration
of the toxin produced can be quite variable. Very low available nitrogen is the
first prerequisite for their growth, but as phosphate limitation increases also,
the toxin production intensifies. (Lassus et al, 1995) When biotoxin production
is viewed as a systemic strategy to remobilize basic nutrients that are tied up
in larger marine organisms, this seems to make sense. As the nutrient
availability becomes ever lower, the system increases the activity of the
homeostatic mechanism designed to counteract the state of extreme depletion:
This natural killing of larger marine organisms such as fish, mammals and
seabirds, will tend to replenish both dissolved nitrogen, phosphate and
zooplankton production, since the corpses will normally be consumed by benthic
scavengers (like echinoderms, extraordinary zooplankton rebuilders) or
decomposed by bacteria which results in the liberation of the basic nutrients in
dissolved form into the seawater.
Marine biotoxin formation under low ambient nitrogen concentrations can
therefore be seen as analogous to the hormones released in mammals when blood
glucose concentration starts to drop - in our case glucagon is released by the
pancreas which causes a prompt release of carbohydrates stored in the liver, and
an increase in blood glucose to the normal level. Homeostatic mechanisms, both
of these. Interestingly, marine invertebrates are immune to the lethal effects
of marine biotoxins, although they are the major consumers of phytoplankton. In
fact, lowly invertebrates often act as the vehicle of transmission of the toxins
to organisms that feed at higher trophic levels…and this reflects the relative
importance of maintaining each of these populations in the ocean.
The second route by which the ocean ecosystem remobilizes nitrogen bound in
temporary storage is accomplished by the selective starvation of the larger
individuals within longer lived, larger species. This is manifested by an
increasing contraction of the age structure of multiple fish stocks, and can
also sometimes be seen in the declining physical health and condition of the
oldest remaining individuals. As with deaths by biotoxins, these natural
starvation deaths result in the nutrients stored within the corpses becoming
available for cycling at lower levels, thus contributing to homeostasis of the
Analogous to body fat on the human body, the existence of a substantial number
of large living fish amounts to a safety margin, a reserve that can be tapped as
needed to sustain the essential process that keeps the very system alive, the
maintenance of the normal biochemical constituency and "cell counts" of
A biological entity, whether a single human or the world ocean, that possesses
just the bare minimum of reserves (i.e. is very thin) is much less resilient to
stresses that will naturally be experienced in the environment. The person with
no fat reserves will continue to maintain normal blood chemistry and blood cell
counts until the starvation problem becomes very acute…and potentially terminal.
This is also true for the dissolved nitrogen and basic plankton parameters in a
‘starving ocean.’ Homeostatic mechanisms work to ensure consistency in the
makeup of the ‘lifeblood’ in each case until the point of total system collapse
A few more comments on "fat":
Beyond functioning as a basic energy reserve in the human, body fat is a dynamic
living tissue that offers other positive benefits to the organism. In the human
example, fat acts as a thermal insulator and is also involved in complex
hormonal processes. The complete physiological significance of body fat is not
yet understood. This undoubtedly also applies to the ocean’s equivalent to
‘fat,’ which to a significant extent consisted of large spawning fish. The
biggest, oldest spawners grew only very slowly, yet they produced the greatest
numbers of fish eggs, and also the greatest mass of spawn by comparison to their
own body size ("GSI"). Therefore, the largest fish were more intensely involved
in cycling nutrients directly into the zooplankton in the form of their spawn.
However, in leaner times these have become too expensive to maintain, and they
have been ‘liquidated’ by starvation and the responsibility for zooplankton
production placed more heavily on the "lower" bottom-dwelling invertebrates
which function more efficiently for the purpose. The largest spawning fish were
often observed to follow the longest migratory routes in some species. And it is
likely that migratory behavior of fish has also played an important, if subtle,
role in marine nutrient cycling patterns…maybe another bit of the complexity of
interdependency that we have failed to appreciate…
4. THE STARVING OCEAN: A MEDICAL DIAGNOSTIC* MODEL
(* The signs, symptoms and diagnostic tests discussed in this section do not
indicate the root cause of systemic starvation, but just help to confirm the
presence of the condition. Examining the history of factors that have impacted
on the ocean will help to establish cause.)
Based on the model of a starving aquatic population (Powell et al, 1995) and the
preceding discussion on homeostatic mechanisms that stabilize the supply of
nitrogen in seawater, it is suggested that observing the following signs,
symptoms, and laboratory findings will be useful in screening for the
possibility of systemic starvation in large marine ecosystems. Also discussed
are the key points leading to differential diagnosis between systemic nutrient
loss and other possible pathologies.
I - ESSENTIALS OF DIAGNOSIS:
(1) A decline in the maximum sizes of fish.
From the model of starvation it is clear that this is the only early warning
sign. Since this effect is also caused by fishing, examining unfished
populations for this trend is necessary. Steadily declining sizes in unfished
populations represent the nearest possible indicator to a "gold standard" sign
of declining marine primary productivity. (Also, the maximum size obtainable by
individual fish in unfished populations therefore represents a reasonably useful
index of total production.)
Regarding the cause of a decline in the maximum size of fish, this must be
differentiated from overfishing. The key to the differential diagnosis between
systemic starvation (food limitation) and overfishing is the condition factor of
the oldest living age cohorts. In starvation, this will be observed to decline,
while in classic "overfishing" alone, the condition factor in these fish will
remain stable or increase. Changes in growth rates have often been seen to
reflect similar changes in condition factor. Declining growth rates and
declining condition factors both suggest increasing food limitation, but
condition factor is the better test since it is much less likely to be under
genetic control than is growth rate. (Genetic change has been suggested,
although never proven, as a possible cause of slowed growth in heavily fished
populations. Condition factor is also affected by "density dependent" effects
however, so declining condition in the context of low abundance is the strongest
signal of starvation.)
(2) A "down the web" shift across species affecting community composition will
also be predicted as the overall scope of the ecosystem contracts.
This signal can also be confused with the effects of overfishing, as in the
model. A shift toward smaller organisms, organisms with lower nutrient
requirements and more primitive species will be expected since these were the
organisms that originally survived in the young ocean, millions of years ago,
during a time when the total marine organic accumulation was less and the rate
of nutrient cycling in the sea was therefore also lower. Therefore, be alert for
a rising presence of cyanobacteria, jellyfish and crustaceans in the ocean.
(3) Records of declining rates of productivity may be discernible in individual
members of long-lived species.
For example, the baleen of the bowhead whale offers a useful record, as has been
documented by one scientist who determined from analyzing bowhead baleen that
productivity in the Bering Sea has declined steadily since at least the mid
1960s. (Schell,D.) Many other organisms may prove to be similarly useful for
(4) Shifting ranges and growth rates in intertidal organisms, especially visible
in sessile perennial forms, will reflect the adjustments of these species to the
declining availability of nutrients. (See articles on this
website outlining changes in barnacles and seaweed.) The exact range shifts
will be determined by the natural gradients of food availability in the
environments of these organisms. Similar range shifts, contracting toward the
areas offering relatively better feeding opportunities, may also be seen in
mobile marine species.
(5) An increasing prevalence of cyanobacteria will be noted, planktonic and
benthic forms both. Accelerated nitrogen fixation is a normal homeostatic
mechanism that occurs in response to lowered systemic nitrogen availability.
Under ‘systemic starvation,’ this activity will be significantly increased.
(6) Laboratory testing will indicate an increase in the biotoxin content of
seawater, reflecting the acceleration of another homeostatic mechanism designed
to correct for nutrient deficiency in the system. Biotoxins produced in the open
ocean more convincingly suggest systemic nutrient loss. Those occurring in
polluted estuaries may be partially stimulated by alterations in N:P ratios.
(7) A decrease in the age and size of marine organisms that produce pelagic eggs
and larvae. There is no proof of this, but it is hypothesized that in a system
designed to maintain stable conditions for life, that plasticity of age at
maturity in these species might function to stabilize the supply and abundance
of zooplankton. If so, declining age at maturity would be expected to accompany
a decline in zooplankton abundance and the signal will be found across all
spawning species, regardless of the intensity of their fishing histories.
(8) A rise may be detected in the concentration of atmospheric CO2. (Shaffer,
1993) (For elaboration on this point see:
** THESE NEXT THREE SIGNS ARE MORE SERIOUS -- If these signs occur, they
indicate the occurrence of "decompensation," a condition where the activation of
the normal compensatory mechanisms has failed to maintain stability within the
system. At this point, many things may unexpectedly go awry. (An analogy from
human medicine would be the development of "shock" symptoms, which indicate a
severely fragile state of health, and one which does not last long. The "shock"
patient either receives prompt, appropriate treatment and recovers, or dies.)
(9) Decline in the stability of the biochemical makeup of seawater.
As biological control mechanisms fail, the nutrient pulses triggered by physical
forcing patterns will become exaggerated. In the North Atlantic ocean, for
instance, the springtime high nutrient levels may reach greater concentrations
and be lowered more slowly by a diminished food web. Similarly, the normal
summertime lows will be exaggerated and dip to lower levels. Chlorophyll
concentrations will also roughly follow this pattern. An increase in the
intensity and duration of the spring phytoplankton bloom, as measured by
chlorophyll content, is therefore not an indication of good health and "high
productivity" in the ocean, but rather the reverse.
(10) A decline in the abundance of zooplankton.
A significant drop in zooplankton is a very grave sign, as this component is
vital to sea life. Rather than representing the second stage of a production
pathway ("secondary production"), zooplankton more correctly represents the
essence of marine animal life.
(11) A decline in unexploited lower non-planktonic organisms.
Declines in organisms such as benthic invertebrates, large populations of which
are critical for the maintenance of zooplankton numbers and the rapid recycling
of bottom organic matter back to the photic zone, will eventually occur. In the
earlier stages of system decline, however, the abundance of these forms may
increase as a greater proportion of phytoplankton production sinks to the bottom
in the absence of the previous level of zooplankton grazing. If these benthic
populations are seen to follow the pattern predicted by the starvation model for
oysters, however, and have reached the point of rapidly declining numbers, this
suggests that the condition of systemic starvation is at an advanced stage.
II. MAJOR CONSIDERATIONS IN THE DIFFERENTIAL DIAGNOSIS OF SYSTEMIC STARVATION IN
Besides checking the condition factor and growth rates of the oldest
individuals, and looking for similar changes in co-existing unfished species,
points which have already been discussed, it bears mentioning which diagnostic
tests are of very limited or no usefulness in distinguishing between overfishing
and systemic starvation. These include assessments of "total biomass," "spawning
stock biomass," the abundance of juveniles, and condition factors or growth
rates averaged over entire populations. None of these parameters will reliably
change during the early stages of population starvation. They will all decline
precipitously in the latest stages, however.
(2) POLLUTION - CHEMICAL
This should usually show more intense effects closest to the pollution source,
except for the longest acting pollutants. Beyond this, although it would be
expected to sicken or kill individual organisms, chemical pollution would not
normally be expected to trigger the onset of gradual changes across the entire
ecosystem that are consistent with a decline in overall system productivity.
Chemical pollution is generally not considered to have had any significant
impact on marine life in the open ocean.
(3) POLLUTION - NUTRIENT
Excessive nutrient loading of estuaries and coastal waters has increasingly
become a focus of concern in marine science, but differentiating between
systemic starvation and nutrient overload can be surprisingly difficult. A
cluster of signs has been associated with intense eutrophication: elevated
dissolved nutrient levels, elevated chlorophyll levels, increased turbidity,
hypoxic/anoxic bottom waters, increased dominance of filter feeders, decreased
growth of larger, perennial macroalgae, and increased growth of smaller,
short-lived macroalgae. (Schramm and Nienhuis, 1996) Some of these diagnostic
tests have more value than others, but, unfortunately it seems too often as if
the appearance of any one of them is taken as conclusive evidence that "eutrophication"
is occurring. And in some situations contradictory signals exist, such as
increased short-lived macroalgae accompanied by a decline in filter feeders. A
critical look needs to be taken at each of these diagnostic tests for
eutrophication to determine its accuracy and usefulness in correctly identifying
instances of true nutrient overload of seawater.
The "specificity" and "sensitivity" of each test needs to be considered. This is
the manner in which the usefulness of medical diagnostic tests is determined.
The "gold standard" test, if it exists, is 100% specific and 100% sensitive to
the condition being tested for. Tests with high sensitivity but low specificity
will give many false positive results, while tests with high specificity and low
sensitivity will give many false negatives. Neither of these extremes represents
a useful diagnostic test.
(a) Elevated dissolved nutrient levels. - This test is very sensitive to
eutrophication but may also sometimes test positive in systemic starvation as
the ability of the living web to dampen natural nutrient pulses is gradually
lost. Therefore specificity of this test is not perfect. Extremely high readings
however, are most likely true reflections of eutrophication, while smaller
degrees of elevation remain questionable.
(b) Elevated chlorophyll levels. - This test is also highly sensitive to
eutrophication (occurs in all grossly obvious cases), but similar criticisms
apply to chlorophyll levels as to nutrient levels. In a starving system that
experiences higher and more prolonged dissolved nutrient pulses from physical
forcing, elevated chlorophyll levels would be expected to follow. (Note the
increasing intensity of "greeness" of the North Atlantic spring phytoplankton
bloom (DFO, 2000, SSR G3-02)…by no stretch of the imagination can this be
considered a reflection of "eutrophication.") Another factor that weakens the
usefulness of chlorophyll levels is the fact that not only all forms of algae,
but also cyanobacteria use this pigment. Cyanobacteria thrive when dissolved
nitrogen is low and can ‘self-fertilize’ by nitrogen fixation. Therefore the
simple presence of a particular level of chlorophyll does not accurately reflect
levels of nutrient input from terrestrial sources. (Note: increasing levels of
chlorophyll have been noted over Australia’s Great Barrier Reef - and this is
known to be the result of the increasing abundance of Trichodesmium in
the seawater. Trichodesmium is a common marine planktonic form of
cyanobacteria, all of which grow best in nitrogen-depleted media.) Therefore
simply looking at chlorophyll levels is a very poor test for nutrient overload
of seawater. It may be a helpful indicator if used with other tests, but is
unreliable if used alone.
(c ) Increased turbidity/decreased light penetration (lowered secchi disk
values). This test is highly sensitive to eutrophication and should rarely
occur in marine systemic starvation, with the possible exception of during
seasonally forced spikes in nutrient and chlorophyll levels, if these become
intense. If this tests positive throughout the entire year, however, it becomes
more specific for the detection of true cases of eutrophication.
(d) Hypoxia or anoxia of the bottom layer of the water column. Again, this
test is highly sensitive for severe eutrophication, but may occasionally give a
false positive in the instance of a severely starved ecosystem in which the
living web can no longer effectively absorb seasonal natural nutrient pulses.
The natural nutrient pulse could result in a heavy bloom of phytoplankton which,
if not processed by a normal zooplankton assemblage, might form a heavy enough
deposit on the seabed that bacterial decomposition might induce hypoxia. (Note:
An incident that occurred off Africa early in 2002 may represent an example of
this type of scenario. Nutrients raised by natural upwelling currents triggered
an intense diatom bloom, which fell to the bottom in such quantity that
oxygen-depleting decomposition became prominent. According to media reports,
lobsters then crawled ashore "gasping for oxygen." It bears keeping in mind that
natural nutrient inputs may eventually appear to be ‘too intense‘ if the marine
food web is drastically weakened. And signals may appear that are
indistinguishable from eutrophication, except for their distance from
anthropogenic inputs. One media report of the events off Africa is posted online
(e) Increased growth of filter feeders.
It has frequently (maybe consistently) been noted in areas of grossly obvious
nutrient overload that filter-feeding organisms that thrive on particulate
organic matter, become relatively more dominant in the environment. (Schramm and
Nienhuis, 1996) In temperate intertidal zones these are commonly found to be
mussels and barnacles. These organisms are good indicators that high nutrient
availability persists year round, since individuals commonly live for several
years. In an environment with a generally declining level of overall nutrient
cycling, however, a decline in the growth of these organisms will ultimately be
expected. The ‘filter feeder test’ for eutrophication is therefore unlikely to
give false positive results and possibly represents the single most valuable
test for the syndrome. Research on marine nitrogen cycling has indicated that:
"Low N-loading rates tend to produce systems in which biomass is dominated by
benthic plants and their associated predators, whereas high N-loading rates
favor dense plankton concentrations and a benthic community dominated by filter
feeders." (Carpenter and Capone, 1983)
This observation suggests the shifts that would be predicted to occur if an
environment were to shift from a relatively high to a lower N-loading regime (an
increase in seaweed and a decrease in filter feeders). It also seems to indicate
that filter feeders represent a much stronger test for "high N-loading rates"
than does macroalgae in general. A close look at macroalgae is warranted
(f) Decreased growth of large perennial macroalgae. Significant declines in
the larger seaweeds, specifically the kelps and fucoids, have been noted to
occur in many marine areas that have received marked increases in
terrestrial-source nutrient input. Some of the best known examples are in the
Baltic Sea. (Schramm and Nienhuis, 1996) One common observation in these areas
is that the fucoid belts no longer extend to the depths that they did
previously. The reason for this is believed to be the decreasing light
availability in the deeper waters caused by increased shading by the dense
growth of phytoplankton. And this is entirely plausible.
However, surprisingly perhaps, a situation of declining nutrient availability to
macroalgae would also predictably induce a loss of the lower part of the natural
range of these plants. The deepest living plants adapt to the lower availability
of light by accumulating a greater concentration of light-harvesting pigments. (Lobban
and Harrison, 1994) Nitrogen is essential for the formation of the pigments, so
the deepest living specimens have naturally a higher nitrogen requirement that
plants situated in areas with greater light availability. And therefore, the
deepest plants are also likely to disappear first in the case of systemic
A useful signal exists however, to distinguish between the two distinctly
opposite possibilities for the disappearance of macroalgae from the deeper
areas. In the case of eutrophication/shading, the marginal, stressed plants
should not give signals of nutrient shortage, but of intensification of
pigmentation before tissue breakdown due to inadequate light. Uptake of
nutrients should not be at the root of the problem in these cases, as it is a
given that nutrients are present in excessive amounts in these environments.
In various species of macroalgae, differing signals may be checked for, based on
the differing internal physiological processes in the plants. Fucoid seaweed
species, for instance, have a very high demand for nutrients at the growing
tips, and they have the capacity to translocate nutrients and products of
photosynthesis from the mature, non-growing tissues to the actively growing
tips. (Lobban and Harrison, 1994). A signal of nutrient deficiency in these
plants, beyond the possible occurrence of lower degrees of pigmentation, would
quite plausibly be an extreme draining of the reserves in the mature tissue to
support the new growth at the tips. A pattern of extreme withering and loss of
mature tissues in
Fucus species has been observed in plants growing along the unpolluted
Atlantic coastline of Nova Scotia (see the seaweed articles on this website,
this one which illustrates the pattern of accelerated loss of mature
tissue). This pattern has also been commonly seen in other areas (New England,
the U.K., the North Sea…personal communication from members of the Algae-L
listserver). This seems to be an important signal, the presence of which should
help determine whether the problem faced by the seaweed is ‘too much’ or ‘too
little’ nutrient availability.
(g) Heavy growth of smaller, short-lived macroalgae. Thin, sheet-like
macroalgae, along with many filamentous algal forms, are commonly noted to
thrive in heavily nutrient-polluted estuaries, and have come to be considered
"symptomatic" of eutrophication. (Schramm and Nienhuis, 1996) This test appears
to have high sensitivity but very low specificity, since the algal types
involved naturally occur across very wide ranges, including the naturally
oligotrophic tropical waters. Very adaptable, these "opportunistic" algal forms
can take advantage of short nutrient pulses (as may occur seasonally in a
starved temperate zone). They can also quickly colonize habitat that has become
available due to the disappearance of longer-lived organisms, and can benefit
from the reduction of longer lived grazing animals which will predictably also
occur in a starved system. Ulva, Enteromorpha and Cladophora species are all too
often taken to offer proof of eutrophication by the fact of their very presence,
but the specificity of this finding to genuinely nutrient-overloaded waterways
is very low. Without exception, these plants have very fine structures and
resulting high SA:V ratios, a plant morphology that gives a natural advantage in
low nutrient conditions. (It is possible that biochemical analysis of some of
these plants may become a useful indicator, but a simple presence/absence test
gives virtually no useful information for the purpose of distinguishing nutrient
overload from nutrient deficiency.)
From this discussion the conclusion emerges that it is surprisingly difficult to
distinguish between a "nutrient-overloaded" and a "nutrient-starved" marine
system. Many of the common tests used today are prone to giving false positive
results. The most important point of distinction probably lies in the
observation that the starved system (in temperate zones) will only give false
positive signals of nutrient overload on a seasonal basis. In a temperate area
where many or all of the symptoms associated with eutrophication persist year
round, and include especially a relative dominance of filter feeders, a genuine
problem of nutrient overload undoubtedly exists, especially if the area is
situated near an obvious source of concentrated terrestrial input. If the signs
appear only on a seasonal basis however, or if only one or two of the less
specific indicators is noted, a diagnosis of eutrophication cannot be made with
any certainty. High nitrogen, elevated chlorophyll, increased turbidity,
dominance of filter feeders, and hypoxia appear to be the strongest true
indicators (all of these have higher specificity than the simple presence or
absence of particular species of macroalgae) and if these tests are positive
throughout the entire year, this probably qualifies as the "gold standard"
diagnostic test for harmful degrees of anthropogenic nutrient input in marine
Are subtle, harmful degrees of eutrophication negatively affecting coastal
waters? It is doubtful if this could occur, since the living marine ecosystem is
well designed to deal with, and even benefit from, smaller pulses of nutrient
input from terrestrial sources as well as those resulting from natural upwelling
patterns. "Subtle" effects of eutrophication on coastal waters may unfortunately
be indistinguishable from the effects of systemic starvation of coastal
waters…and if researchers are only seeking eutrophication, they may mistakenly
believe that that is what they have found…
(4) CLIMATE CHANGE
Changing climate variables can cause changes in levels of marine productivity.
Specifically, declines in the "carrying capacity" of ecosystems is recognized as
one potentiality. (Beamish, 1995) This has been convincingly proven, especially
so in the Eastern Pacific ocean, where predictable shifts in fisheries
productivity have been related to ENSO patterns. These fluctuations may,
however, be superimposed upon a subtle underlying theme of steady background
decline due to nutrient loss.
In any case, the distinction between "climate change" and "systemic starvation"
can probably best be made in areas not significantly affected by climate change.
The Northwest Atlantic ocean presents a good example. Dramatic collapses have
occurred in fish stocks that simply have not been accompanied by any impressive
degree of climate change. In analyzing the reasons for the collapse of the
Northern cod stock, Hutchings and Myers convincingly rejected the hypothesis
that it might have been triggered by climate change. (Hutchings and Myers, 1994)
General predictions of the effects of climate change on marine populations also
include the thought that species may expand their ranges poleward. Range shifts
occurring in many species today are not always poleward. A good example is the
Northern cod, where the remaining concentrations of these fish are now found in
the parts of their former range that have the highest natural nutrient
availability (inshore in a few bays of Newfoundland, in the Northern Gulf of St.
Lawrence, and on Georges Bank). Incidentally, none of these cod populations are
showing any convincing signs of "rebuilding."
Poleward range shifts have been noted as well though. One well documented study
of a western North American intertidal community demonstrated, over a period of
70 years, a significant decline in species classed as relatively "northern" and
a corresponding increase in "southern" types. (Barry et al, 1995) Regarding this
change though, it bears pointing out that the "southern" types might be more
naturally adapted to lower nutrient regimes as well as to higher temperatures,
by comparison to the "northern" types. Teasing apart the relative importance of
the possible causes of these community shifts may be difficult.
(5) NATURAL PREDATOR IMBALANCE
People in some areas are convinced that natural predators are harming fish
stocks, and preventing their rebuilding. Examples are the fishermen and
scientists in Atlantic Canada who insist that a seal cull is necessary to allow
the cod to grow out of the "predator pit" that they believe the seals holding
them in. Similarly, it is believed by some in Japan that whales are harming the
fish stocks there.
Differentiation between a starving ecosystem and an overabundance of natural
predators can be aided by checking two important parameters of the prey
population. The first is the growth rates and physical condition of the largest
prey individuals. If these are found to be in poor condition, population
starvation must be suspected. If the largest prey fish are in high condition,
however, overexploitation by natural predators might be a possibility (although
overexploitation by humans is a more likely scenario since the ecosystem has
checks and balances built in to avoid the accumulation of an overabundance of
any natural marine predatory species). The other factor that must be assessed is
the food supply available to the prey fish population. For most fish, the
abundance of zooplankton will be a significant indicator of their food
availability. If a given level of zooplankton has been associated in the past
with a greater growth of the prey fish, then overexploitation by predators might
be limiting the growth of the fish population. If, however, zooplankton levels
are at historic lows, then systemic starvation may be the limiting factor on the
growth of the fish. And zooplankton is clearly declining in many parts of the
world ocean. (Northwest Atlantic: DFO, 2001, California: Roemmich and McGowan,
1995, North Sea: Parsons et al, 1984).
(6) ULTRAVIOLET RADIATION
Ultraviolet radiation occurs naturally and is capable of causing damage to many
organisms, plants and animals alike. In recent decades ultraviolet radiation has
increased measurably, particularly at the global poles, and the question often
arises of whether this increase might be causing damage to marine life. This is
theoretically possible, but a few arguments can be made to show that increasing
UV radiation is probably not a major cause of the widespread declining trends in
First, the increasing intensity of UVR has been concentrated at the poles of the
planet. Declining patterns in tropical marine life are, however, as impressive
as those that have occurred in the temperate and polar regions. (Jackson et al,
Secondly, it will need to be determined at which point in the food web that the
radiation damage is being done. Superficially, at least, UVR does not appear to
be inhibiting the growth of the phytoplankton, since satellite pictures are
showing increasing degrees of "greeness" in many ocean areas. The level of the
zooplankton - this is definitely dropping, and it seems as if the damage to the
web is occurring on this level. Zooplankters might be naturally vulnerable to
damage by UVR, but to quite an extent they follow a behavior pattern of avoiding
intense sunlight. Zooplankton are known to undertake substantial daily vertical
migrations in the water column. The typical pattern is to rise to the surface
layer at night to feed on phytoplankton, and then to swim down to much deeper
levels during the day. Most of their daylight hours are therefore spent more or
less ‘in the shade.’
Lastly, it appears that the declining trend in marine productivity has been
going on for a much longer time than has the rising trend in UVR. The maximum
sizes obtained by many marine species, for instance, seems to have been dropping
for many more decades than UV has been rising. Fisheries had already experienced
significant declines before humans began releasing CFCs into the atmosphere. (Mowat,
1984, Jackson et al, 2001) UV radiation might be inflicting damage on some
marine organisms today, but it is not credible as a major causative factor that
is forcing the general decline. A plausible "cause" must be seen to precede the
appearance of the presumed "effect."
5. THE EARTH’S OCEAN TODAY: A HISTORY AND PHYSICAL EXAM, AND SUMMARY OF CLINICAL
Extremely old, life in Earth’s ocean has experienced a few ups and downs before
this time. On past occasions marine life has recovered from mass extinction
events, albeit this recovery has been very slow by human time scales. The
presently existing assemblage of marine organisms evolved over recent hundreds
of millions of years, and has seemingly maintained a fairly stable composition
and level of productivity for thousands of years prior to the present time.
Over the last 1000 years, predation on marine life by terrestrial mammals has
risen to an unprecedented level. Virtually all larger marine species have been
targeted by this predation, although there was a tendency at first to target the
very largest species and those organisms living at highest trophic levels.
Massive declines have occurred in the populations of targeted species, which has
also affected many unexploited species due to altered patterns of species
interactions. (Jackson et al, 2001)
Major physical findings today, with a consideration of a possible diagnosis of
Ideally considered in an initial assessment perhaps, is the Canadian section of
the Northwest Atlantic ocean, a large marine ecosystem that has not experienced
a significant degree of climate change to date, but has been the subject of a
substantial degree of scientific investigation. Major changes have occurred in
the biota of this part of the world ocean, and it can be demonstrated that these
changes are essentially consistent with the starvation model and anticipated
‘homeostatic’ responses. Significant evidence includes:
- A decline in the maximum sizes of fish has occurred. (e.g. Pauly et al, 1998)
- A "down the web" shift in species composition has occurred (areas formerly
dominated by fish are now dominated by crustaceans - this is well known, but a
more subtle "down the web" shift has also occurred in unexploited species such
as those occurring in the intertidal zone - see the articles on
barnacles and seaweed posted on this website.)
- Ranges of some species have visibly contracted into the areas where nutrient
availability is naturally relatively higher (as discussed in earlier sections of
- An increasing frequency and extent of harmful algae blooms has occurred. (Lassus
et al, 1995)
- Declining age and size at maturity has been noted in all species for which
this data has been collected. Besides groundfish and pelagic fish, this trend
includes crustaceans such as lobster, crab and shrimp. (DFO…all recent stock
status reports are available online at www.dfo-mpo.gc.ca/csas/csas/ )
- An increasing intensity and duration of the spring phytoplankton bloom has
been recorded in recent years. (DFO, 2000c, DFO, 2001)
- A declining trend in zooplankton abundance has occurred. (DFO, 2000c, DFO,
The declines in marine life in Atlantic Canada have been largely attributed to "overfishing,"
therefore this is the differential diagnosis that needs to be most carefully
made. Three fish species will be considered in more detail: Northern cod,
capelin and Atlantic mackerel.
(1) Northern cod.
Although difficult to ascertain from early fishery records (which mostly have
included only tonnage landed), it appears that the decline in the maximum size
of cod occurred over many decades. The decades during which fishery statistics
included biological data (approx 1960 - present) roughly indicate that a steady
decrease in the maximum age and size of cod occurred throughout this time. But
was that the result of direct fishing pressure applied to the cod stock, or to a
lowering of the scope for growth of cod in the ecosystem? Records on the cod
stock include growth indices (although not commonly condition factor) for
individual age cohorts, and these records show declining growth indices which
occurred, at the outset, more steeply in the oldest ages and not at all in the
younger ages. This trend immediately preceded the disappearance of the older
ages of fish from the data tables. (Lilly et al, 1999) Both the precipitous
nature of the population collapse, and the failure of the cod stock to recover
under a prolonged fishing moratorium, are suggestive of systemic starvation or
"bottom-up control" as a major underlying factor that has forced this decline.
Indices of cod growth continue to decline in Atlantic Canada, seeming to
indicate a further steady lowering of the scope for fish growth and productivity
of this ecosystem. (Although the groundfish fisheries have been scaled back
greatly in recent years, they have not been eliminated, and large amounts of
marine biomass extraction still occurs in the form of crustaceans - a practice
that "might" also further hamper nutrient cycling and productivity of the
system… "if" fishing is implicated as a cause of the problem.)
Although the sequence of events that has occurred with the Northern cod is
consistent with the starvation model, this stock has been subjected to centuries
of intense fishing, and the suspicion will remain that the cod reacted
ultimately only to the recent cod fishery, rather than to a more subtle and
longer-term ecosystem effect (which ‘might’ still be an effect of fishing, but
via a longer-term and slightly indirect route). If the forcing mechanism that
caused the cod collapse was a relentless lowering of scope and production in the
overall ecosystem, then lightly exploited and unexploited species in the same
area must also show the same trend. Unfortunately, detailed time-series
biological records have not been kept on unexploited species (with the partial
recent exception of plankton), but a similar pattern of decline can be
demonstrated in two lightly fished commercial species, capelin and mackerel.
This small, cold water pelagic "baitfish" is a major prey species for cod, other
predatory fish, marine mammals and seabirds. Fisheries exploitation of capelin
has been at such a low level compared to natural predation, that it is believed
that no biological effects could have been exerted on the capelin stock by the
capelin fishery per se. (Carscadden et al, 2001)
Unexpectedly, however, capelin has declined as its major predator (cod) has
disappeared. Once a vast population of capelin existed on the offshore
Newfoundland shelf, but now only a remnant remains there. (acoustic survey, DFO
2000a, Carscadden, 2001) The remaining concentrations of capelin, as with the
cod, are now located in nearhore waters.
Declining biomass aside, have the signals of population starvation appeared in
the capelin stock? Recent assessments on capelin in Atlantic Canada have
recorded mature fish aged 2 - 4 years old (DFO, 2000a, Carscadden, 2001) while
older references describe mature capelin as commonly living to age 5 years, with
a maximum observed age of 7 years. (Leim and Scott, 1966) The maximum age of
capelin appears to have been lowered. In recent decades scientists have
documented a decrease in the average size of capelin, as well as a population
shift towards a higher proportion of younger fish in the spawning population.
The average age at first maturity is also dropping significantly. And the
reasons for these shifting trends are "unknown." (DFO, 2000a) Data on condition
of capelin is sketchy beyond the observation that they are generally smaller now
than they have historically been known to be. The specific signal of declining
condition in the older ages of capelin cannot be detected although it may
certainly be part of the general decline in size of fish. Age contraction of the
stock (the single early signal of food limitation) and declining age at maturity
(a hypothetical signal of declining productivity), however, seem consistent with
the possibility of an increase in bottom-up control of capelin.
(3) Atlantic mackerel.
A migratory schooling pelagic fish that historically lived to 20 years, the
Atlantic mackerel ranges from Newfoundland to North Carolina. The stock
component appearing in Canadian waters has experienced a rapid contraction of
its age structure over the last few years (based on assessment of commercial
catches, DFO, 2002). In recent years, directed fishing pressure on the mackerel
stock has been considered to be relatively light, so "overfishing" can plausibly
be ruled out as the cause of this change. It has been believed by some
scientists that exploitation rates on mackerel could safely be increased (Overholtz,
2000 (NMFS)). Yet, at least on the Canadian side, mackerel stock assessments are
revealing alarming signals of a decline, one which cannot be clearly related to
the mackerel fishery itself. For example, estimates of spawning biomass have
dropped substantially "…between 1993 and 1996 inclusive, the spawning biomass of
mackerel in the Gulf apparently dropped from 936,000t to 126,000t, a difference
of 810,000t. During the same period, reported landings for eastern Canada were
only 85,376t…" (DFO, 2002)
But spawning biomass is not the critical signal when assessing for the
possibility of a starvation-induced population decline. What is the recent trend
for the age structure of the Atlantic mackerel stock?
Figure 6. Canadian catch at age (%) for mackerel during the 1973-2001 period
(the year-classes that have dominated the fishery for several years are
indicated; age group 10 represents all fish aged 10 or over). (DFO, 2002)
File courtesy François Grégoire
The "catch at age" data (at right)
suggests a rapid decline in the maximum ages reached by mackerel. Fish aged 10
years and older were once routinely found in the catches, but last appeared (in
numbers great enough to warrant a blip on the graph) in 1998. In 1999 and 2000
the maximum age was recorded at 6 years in the "catch at age" data, and in 2001
it dropped again to 5 years.
Trends in age at maturity and condition factor data by age cohort have not been
reported in the scientific assessment of the mackerel stock, but the essential
signal seems to be loud and clear: The only early warning signal of the onset
of population starvation is the loss of the older, larger individuals.
The big mackerel are not being harvested by fishermen, it appears possible that
they are now being "harvested" by the ocean herself. In all likelihood the large
mackerel are now dying of starvation and their nutrients are being recycled in
the larger systemic effort to maintain stability of the plankton and the supply
of dissolved nutrients in seawater.
The trajectory of the recent decline in the age of mackerel is so steep that
stock extinction appears to be imminent. This collapsing trend echoes the steep
contraction in age structure that accompanied the collapse of Northern cod a
decade ago. The cod however, has so far managed to continue to linger and
survive in some near shore refuges. This coping mechanism will not likely work
for the mackerel stock however, due to its long migration pattern and affinity
to warmer waters. A few mackerel may manage to linger at the continental shelf
break, where upwelled nutrients and warmer water may sustain them for a while,
but it is very doubtful that a successful spawning outcome for mackerel could
occur without following its traditional pattern of inshore migration. The
prognosis for Atlantic mackerel now looks very poor.
For how long has the Atlantic mackerel been affected by the "lowering of the
ceiling?" Long term data is sketchy, but the insidious decline and loss of the
larger fish appears to have spanned many more years than just the last couple of
decades. Older scientific references to mackerel in Atlantic Canada state that
they "rarely" were seen at sizes above 4 pounds in weight and 22 inches in
length. (Leim and Scott, 1966) That describes what would be an unbelievably
large mackerel today. Length and weight data on mackerel collected by DFO
scientists from the 1970s till the present indicate that no significant numbers
of mackerel in those years have grown above 2 pounds in weight or 16 inches in
length. (DFO, 2002)
(Incidentally, regarding DFO's Fig 6, "Canadian catch at age" for mackerel, a
lesser contraction in the age structure of the stock was apparent in the 1970s.
The extreme concentration of biomass in the lowest age cohorts did not occur at
that time, however. The 1970s age contraction in mackerel was a reflection of
the effects of "overfishing" which occurred at the time as mackerel were heavily
exploited offshore by a large foreign fishery. The ‘scope for growth of
mackerel’ in the ecosystem had not been lowered so far in the 1970s as it is now
however, and the release of the foreign fishing pressure in 1977 resulted in a
prompt rebounding of the age structure of the mackerel stock. All of these
elements are the same as the tales of the Northern cod and the other groundfish:
they were overfished in the 1960s and 1970s, but promptly rebounded when fishing
pressure was relaxed. Then a few decades later these same fish stocks were
overtaken by a sudden collapse from which they remain unable to recover. This
illustrates, in the first part, the effects of "stock overfishing" on individual
species and in the second part, the effects of "ecosystem overfishing" on all of
At this point, the history and current physical findings offer grounds for a
strong suspicion that starvation is increasingly limiting the potential for
growth of all marine life in Atlantic Canada. Total primary productivity in this
ecosystem appears to be dropping, as indicated by the steady and increasingly
acute loss of all larger fish.
These observations from Atlantic Canada are consistent with findings elsewhere
in the world ocean that seem to point towards the same conclusion: a broad
systemic lowering of "productivity" rates, increasing "bottom-up control" or
"mounting starvation," whichever phrase you prefer…
Observations from other parts of the world ocean include a few interesting
- The problems that have plagued the tropical corals in recent years, epidemics
of disease and mass bleaching and death during warm periods, these developments
offer a picture that is indistinguishable from the scenario that would be
predicted to unfold "if" increasing degrees of bottom-up control were applied to
tropical ecosystems. (See
coral report on this website.) The increasing prevalence of cyanobacteria in
tropical reef communities, including their direct implication in some emerging
coral diseases, is consistent with the general expectation that, under
increasingly nutrient-limited conditions, cyanobacterial growth (and nitrogen
fixation) will increase. And the overgrowth of coral reefs by macroalgae is
consistent with a shift towards lower N-loading rates, as predicted by the
observations of Carpenter and Capone (1983).
- The declining trend in sizes of marine fish and their ages at maturity has
been well documented in the North Pacific as well as in the North Atlantic
ocean. But an interesting aberration from the pattern has also been recorded
across the North Pacific. The size of five species of Pacific salmon, from North
America and Asia, has shown a steady and very substantial decline in average
size over recent decades (Bigler et al, 1996, Helle and Hoffman, 1995). But,
instead of showing the lowered age at maturity, as in the marine fish stocks,
Pacific salmon clearly show the opposite tendency. Age at maturity is
significantly increasing in Pacific salmon stocks (both North American and
Asian) that have been examined for the trend. (Helle and Hoffman, 1995)
How do these changes in salmon compare to the predicted trends in a "starving
ocean" and the hypothesis that declining age at maturity represents a systemic
effort to enhance zooplankton?
Since salmon are not marine spawners, perhaps the imperative to produce spawn at
a younger age in conditions of lowered zooplankton is not felt by these species.
The spawn that salmon produce does not play a part in marine zooplankton.
The size decline in Pacific salmon appears certainly to reflect a decline in
their feeding opportunities, which is consistent with a decline in ocean
productivity. So salmon compensate now by spending more years at sea in order to
accumulate enough stored energy before attempting to ascend the rivers. And they
are tackling the rivers with far lower energy reserves than they did in the
past. For example, populations of chum salmon in Alaska and Washington states
were observed to experience an average body weight decline of 46% between 1976
and 1991. (Helle and Hoffman, 1995)
Salmon appear to be compensating on two fronts for the declining feeding
opportunities in the North Pacific, they have steadily increased their age and
decreased the energy that they store for their spawning migration. One or the
other of these variables may be approaching the physiological limit for survival
of these fish. It is difficult to guess just how close these species are "to the
wall" at present, but in river pre-spawning mortality due to low energy reserves
and high parasite loads seems to increasingly be an issue with some salmon runs.
Warmer water aggravates these deaths, but may not be the real root of the
As with the sudden collapse predicted for the oysters in the model, and the
"crashes" experienced by the Northern cod (and now seemingly the Atlantic
mackerel) in Atlantic Canada, a further slight reduction in marine productivity
of the North Pacific may suddenly eliminate a large portion of these salmon.
Biomass and abundance estimates will not be the biological reference points that
will signal the approaching collapse of Pacific salmon. Monitoring of the base
of their food web, not the phytoplankton but the zooplankton, will be the
single best indicator - and if it continues to drop, the immediate danger to the
salmon may very suddenly become apparent.
A final observation can be made regarding changing trends in age and size at
maturity of marine fish, parameters which are widely declining. A model of
"plasticity for age and size at sexual maturity" in fish has been described in
the literature. (Stearns and Crandall, 1984) This model predicts several
different trajectories along which these parameters may change, depending on
which types of environmental stressors force the changes. If environmental
conditions cause an increase in adult mortality but no change in juvenile
mortality (as in the starvation model of Powell et al), then the model of
Stearns and Crandall clearly predicts that organisms will mature earlier and at
The consistency of these general predictions with the declining trends widely
observed today in the ages and sizes at maturity of marine fish (including
lightly exploited species), further supports the hypothesis that ever-increasing
bottom-up control, or ‘starvation,’ is forcing the changes.
6. CONCLUSIONS: TREATMENT OPTIONS,
PROGNOSIS AND RECOMMENDATIONS
If humans prefer to see marine life
continue to persist as we have come to know it in recent centuries, instead of
witnessing an abrupt "regime shift" to a less productive system dominated by
bacteria, toxic phytoplankton and jellyfish, then we urgently need to change our
approach. We will need to stop aggravating the problem and find a way to asssist
the natural healing mechanisms within the patient, the ‘internal organs’ that
produce and support the zoopankton assemblage. If we prefer to carry on as usual
and watch ‘natural events’ unfold, then it is time now to brace ourselves from
some very nasty surprises.
Major ‘internal organs’ involved in the sustenance of marine zooplankton are the
entire group of organisms that produce pelagic spawn. This fact has been largely
unrecognized in scientific analyses of the workings of the marine ecosystem.
Recognizing this fact now should lead to another urgent rationale to stop bottom
trawling, since this practise destroys key benthic organisms that are important
in nutrient cycling far beyond their role in providing forage for bottom feeding
fish. But stopping bottom trawling will not be enough to halt the declining
trend in marine productivity. Any continued marine biomass extraction that is
not appropriately replaced will further exacerbate the ongoing problem. And ‘the
patient’ has already been brought very low. (Mowat, 1984, Jackson et al, 2001)
If any "treatment" is to be attempted besides stopping fishing, it probably
should be in the form of a solid food subsidy that can be directly consumed by
benthic scavengers and fish, something that can be eaten directly by organisms
that produce pelagic spawn. The simple addition of dissolved nutrients to
seawater will not result in those nutrients being taken up and recycled as
effectively in the larger web. (This particular experimental treatment has
already been well tested, and the dearth of marine life in polluted estuaries
attests to its failure.)
Currently a major international scientific research effort is directed towards
monitoring the ocean to discern the ecosystem effects of climate change (JGOFS).
Detailed investigations are being made into the question of how climate will
affect marine food webs and marine productivity in the future. What is
urgently needed however, and long overdue, is an intensive and objective
scientific inquiry into the effects on marine productivity and marine food webs
that have already been induced by centuries of fishing.
Marine biology now needs to make a quantum leap in thinking. A quick divorce
from the commercial fishing industry and single stock management activities is
necessary, and a wholehearted commitment to the ideals of "conservation" and
"ecosystem health" is imperative for the branch of science charged with the
responsibility of safeguarding the ocean, the original ‘lifeblood’ of this
planet…To do anything less is the equivalent of continuing to use medical
doctors who persist in trying to heal a sick patient by "bloodletting," a
primitive and lethal practise long ago abandoned by scientists as they gradually
became enlightened, over centuries, into the basic principles that govern the
maintenance and restoration of human health. Trial and error in the early days
of medical science often resulted in the unanticipated death of the patient.
Many things in medicine were not at all as they first appeared to be, and the
true functions of many mysterious body parts were only discovered in the later
stages of the study. Many are still not understood. The current level of
misunderstanding and uncertainty in marine science is not the fault of today’s
marine scientists, it simply reflects how young their science is, and how large
and difficult to understand their ‘patient’ is… Unfortunately, marine science’s
first ‘patient’ will also be their last. The consequences of a single fatal
error will be permanent and far-reaching, not only for marine life but for a
great number of terrestrial forms as well.
It is clear that biological systems can withstand and adjust to various levels
of different stressors. They have a natural resiliency. But it is also clear
that any of these systems can be "pushed too far," and will eventually reach a
critical point where major and irreversible changes take place "suddenly."
Earth’s ocean ecosystem is showing multiple signs now that the human fishing
pressure is too intense. "Decompensation" will result in a sudden irreversible
change. It is not possible to predict exactly how soon the permanent ‘downshift’
will occur, beyond noting that it appears likely to happen ‘soon.’
The problem of the ailing ocean is now at a critical point, and marine biology
urgently needs to seek helpful insights from every and any field of human
knowledge that might possibly assist in putting the pieces of the puzzle
together and finding the best solution.
Barry, J. P., C. H. Baxter, R. D. Sagarin, and S. E. Gilman. 1995.
Climate-related, long-term faunal changes in a California rocky intertidal
community. Science 267:672-675.
Bates, Nicholas R. 2001. Interannual variability of oceanic CO2 and
biogeochemical properties in the Western North Atlantic subtropical gyre.
Deep-Sea Research II 48(2001):1507-1528.
Beamish, R. J. (ed). 1995. Climate change and northern fish populations. Can.
Spec. Publ. Fish. Aquat. Sci. 121:739p
Berger, W. H., V. S. Smetacek and G. Wefer (eds). 1989. Productivity of the
Ocean: Present and Past. John Wiley and Sons.
Bigler, B.S., D. W. Welch, and J. H. Helle. 1996. A review of size trends among
North Pacific salmon (Onchorhynchus spp). Canadian Journal of
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Carscadden, J. E., K. T. Frank and W. C. Leggett. 2001. Ecosystem changes and
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