23 DECEMBER 2016 • VOL 354 ISSUE 6319 1529 SCIENCE sciencemag.org
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By Andrew J. Watson
For the past several hundred million years, oxygen concentrations in Earth’s atmosphere have been comparatively high (1, 2). Yet, the oceans seem never to have been far from anoxia (oxygen depletion) and have occasionally suffered major oceanic anoxic events (OAEs),
recognized in the rock record through accumulations of dark, organic-rich shales
(3). OAEs seem to be promoted by warm climates, and some have been associated with
major environmental crises and
global-scale disturbances in the
carbon cycle. New insights into the
causes of OAEs are now emerging
(4, 5). Furthermore, ocean oxygen
concentrations are declining in the
modern ocean (6). A full-scale OAE
would take thousands of years to
develop, but some of today’s processes are reminiscent of those
thought to have promoted OAEs in
the distant past.
Even today, the oceans are on
the edge of anoxia: Every ocean
basin has an oxygen minimum
zone (OMZ) at a depth of a few
hundred meters, where respiration
consumes oxygen and depresses
oxygen concentrations. Over large
areas of the Eastern Pacific and
the northern Indian Ocean, oxygen
levels in the OMZ are close to zero.
In modern times, some OMZs have
expanded, a process called ocean
deoxygenation (6). In addition, nutrient input from rivers has led to
eutrophication and local anoxia in
many coastal regions. An example
of these “dead zones” is the Gulf of
Mexico near the Mississippi Delta, but there
are now several hundred anoxic coastal regions worldwide. Mostly, these are the result
of human activities that have led to much-increased nutrient levels in rivers.
Why is the deep ocean deoxygenating?
Human-caused eutrophication may be a con-
tributing factor, but climate change is also
implicated. Warming promotes deoxygen-
ation because it slows the formation of deep
waters and decreases the solubility of oxygen
in the surface. At a recent discussion meet-
ing at the Royal Society in London, all these
possible causes were discussed (7). Yet, none
of them seems to fully explain the observed
declines in oxygen, especially those seen in
the tropical oceans.
As to the persistence of OMZs in the
oceans past and present, a simple calculation,
first made by Alfred Redfield (8), suggests
that the global ocean is chronically close to
the edge of anoxia. When water leaves the
sea surface, it carries oxygen absorbed from
the atmosphere into the interior. An equiv-
alent volume of deep water must upwell to
the surface, carrying the limiting nutrient
phosphate up from the deep ocean. (The
deep waters must also carry up nitrate, but
geochemists think of phosphate as the limit-
ing nutrient because nitrogen can always be
fixed by plankton from the atmosphere if it
is in short supply.) Photosynthetic plankton
then use up all the nutrients in the upwelling
water, and the fixed organic matter sinks into
the deep sea. There, it is respired back into
inorganic carbon and nutrients by microbes,
in the process consuming the oxygen sup-
plied by the sinking water. Using the stoichi-
ometry of carbon and nutrients now called
the “Redfield ratios,” Redfield found that the
amount of oxygen consumed is almost equal
to that carried down by the sinking water (8).
The oxygen demand in the interior of the
modern ocean is thus constrained to be close
to the oxygen supply. This near-equality seems
paradoxical because demand and supply are
set by two apparently independent variables:
Demand is governed by the amount of phosphate in the deep ocean, whereas the supply
is set by the amount of atmospheric oxygen
that dissolves in surface water. A little more
phosphate, and much more of the ocean
would be hypoxic (low in oxygen). Doubling
ocean phosphate would be sufficient to bring
on a full-scale ocean anoxic event.
Past natural events are believed
to have suddenly increased the
supply of phosphorus, especially
the massive outpourings of magma
that form large igneous provinces
(LIPs). Prominent OAEs occurred
at the same time as, or very shortly
after, the eruption of LIPs (4, 5, 9,
10). A possible mechanism is that
the fast-weathering rocks emplaced by these events increase the
supply of nutrients to the oceans
for thousands of years, forcing the
ocean into anoxia.
Once anoxia takes hold, it may
be self-sustaining. Phosphorus is
removed from the ocean through
sedimentation, but if anoxic waters overlay these sediments they
tend to leach out much of this
phosphorus; in contrast, if the water is oxygenated the phosphorus
stays in the sediments. Sediments
in contact with anoxic water are
thus an inefficient phosphorus
sink and may even be a source of
phosphorus to the ocean. Models
suggest that once anoxia begins
to spread over continental shelves
and slopes, this positive feedback may drive
the ocean into prolonged deoxygenation that
lasts hundreds of thousands of years (see the
figure) (11, 12).
Since the industrial revolution, land-use
changes, agricultural runoff, and sewage discharges have more than doubled the amount
of phosphorus entering the ocean via rivers
(13). The coastal dead zones that have developed as a result are often lethal to animal
CLIMATE CHANGE
Oceans on the edge of anoxia
Environmental crises can tip the ocean into O2 depletion
College of Life and Environmental Sciences, University of
Exeter, Exeter, UK. Email: andrew.watson@exeter.ac.uk
Closing the cycle
Over time periods of 100,000 years or more, the
oceans recover from their deoxygenated state.
Limiting processes
More burial of carbon leads to an
increase in atmospheric oxygen,
causing more wildfres that reduce
forest vegetation (4). This lowers the
phosphorus input to the oceans.
~100,000 years
1
2
3
O2
4
Anoxic
ocean
1
Positive feedbacks
High phosphate inputs (1)
enhance marine production,
reducing oxygen in the OMZ (2).
The resulting phosphorus release
from sediments (3) further
increases marine production and
carbon burial.
~1000
years
Oxygen crises in the ocean
Major environmental crises can lead to oxygen depletion (anoxia) throughout
the ocean’s oxygen minimum zones, which become deadly for animal life.
