commentary

Redfield’s evolving legacy

Nicolas Gruber and Curtis A. Deutsch
The ratio of nitrogen to phosphorus in organic matter is close to that in seawater, a relationship
maintained through a set of biological feedbacks. The rapid delivery of nutrients from human activities
may test the efficacy of these processes.

F
ew ideas have influenced marine ecology several orders of magnitude increase in the chemical environment implies that some
and biogeochemistry more than those amount of data (Fig. 1). But our knowledge form of homeostasis is at work, that is,
first developed by Alfred C. Redfield of the plankton that drive the cycles of N, P feedbacks that stabilize the nutrient content
80 years ago1. Drawing on the observations and other elements, their diverse metabolic against external perturbations. But despite
of his contemporaries, Redfield marvelled pathways, and environmental constraints, decades of research, the exact mechanisms
at the close correspondence between has grown tremendously, with new governing this homeostasis are still not
the proportions of nitrogen (N) and discoveries accruing at a rapid pace. fully understood3,4. It is clear, however,
phosphorus (P) in phytoplankton biomass, Extensive perturbations of the ocean’s that oceanic biota control these feedbacks
and in average seawater. Two essential physical and chemical environment that are and that the N:P ratio of the seawater
features of this correspondence can be now under way hold the potential to greatly must play a central role5. Given that the
seen in the relationship between the major alter the regulatory balance that Redfield main input of P into the ocean by rivers is
abiotic reservoirs of N and P, nitrate and envisaged. These global changes are sure to under geological control and varies only
phosphate (Fig. 1). First, the two nutrients challenge and deepen our understanding on timescales of several tens of thousands
are correlated with a nearly constant slope of the dynamics that have coupled the of years, the central role of the N:P ratio
of roughly 16:1; second, the intercept of elemental cycles throughout Earth’s history. implies that the main inputs and outputs of
that line is very close to zero, meaning that biologically available N must depend on the
the total amount of nitrate and phosphate Redfield’s homeostasis N inventory itself.
present in the ocean also have nearly the Maintenance of the tight stoichiometric Redfield’s original conception of such a
same ratio. relationships between biota and their feedback centred on N-fixing cyanobacteria,
Having made the first measurements of
stoichiometry in phytoplankton, Redfield
easily reasoned that the slope of the a b
50
relationship between these nutrients occurs 16:1

3
NO
because phytoplankton tend to consume 45

ss
these nutrients at a relatively fixed ratio ce
Ex
Denitrification?
(16:1) during their growth. The death and 40
Nitrate

sis

n
io
decomposition of plankton biomass return he

sit
t
yn

po
35
these nutrients to deeper water in the same os
m
ot co
proportion. He was more tentative however, Ph
Nitrate (µmol kg–1)

De
30
in explaining why the total amounts of
nitrate and phosphate follow the same ratio. 25 c
Some 20 years after identifying this ratio2,
he expounded three possibilities: “1) a 20
coincidence dependent on the accidents sis
n
io

15 he
sit

of geochemical history; 2) adaptation on t

Nitrate

yn
po

os
m

the part of the organisms; or 3) organic Pacific ot

co

10
Ph
De

processes which tend in some way to Atlantic N fixation?

Indian
it

control the proportions of these elements in 5

fic
de

the water.”
3
NO

0
Redfield’s arguments gravitated toward 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Phosphate
the latter, and he began to articulate a Phosphate (µmol kg–1)
mechanism — a feedback in modern
parlance — by which the ocean’s biota
regulates the nutrient composition of the Figure 1 | The relationship between nitrate and phosphate in the ocean. a, Observations used by
ocean. Thus the understanding emerged that Redfield in his original study1 (filled circles) and selected data from the global World Ocean Circulation
life and its environment are locked in a state Experiment survey (WOCE; small symbols) show a clear, approximately 16:1 relationship between nitrate
of mutual influence. and phosphate, with minimal deviation. b,c, Both denitrification (b) and N fixation (c) counteract any
The fundamentals of the observations on imbalances, with denitrification removing a nitrate excess, and N fixation adding more nitrate to the ocean.
which Redfield based this conception have Together, these processes are expected to return nitrate concentrations back towards a mean content close
changed remarkably little in 80 years, despite to that of oceanic phytoplankton. Figure adapted with permission from ref. 5, © 2008, Academic Press.

NATURE GEOSCIENCE | VOL 7 | DECEMBER 2014 | www.nature.com/naturegeoscience 853

© 2014 Macmillan Publishers Limited. All rights reserved

commentary

Anaerobic ammonia oxidizers

Atmospheric (anammox), a recently discovered group of
CO2 Climate autotrophs that also remove bioavailable N,
could alter the strength of the N-removal
N inventory
Decreasing

Iron feedback. But because the activity of

deposition anammox is also ultimately limited by the
Low N:P
Export
flux of organic matter through the OMZ,
production the sensitivity of the feedback should be
similar, whether it is classical denitrification
Diazotrophic Thermocline Benthic N or anammox that removes fixed nitrogen.
selection oxygen deposition
The strength of the denitrification feedback
is, however, very sensitive to how strongly
Benthic Water-column Water-column Benthic
denitrification denitrification
N fixation N fixation
denitrification denitrification
ordinary phytoplankton are limited by
nitrogen. In many regions, other factors
such as light and iron are more important
Benthic N Thermocline Diazotrophic
deposition oxygen selection than nitrogen in limiting phytoplankton,
reducing the strength of this feedback. The
Export strength of the feedback would be further
production

N inventory
High N:P

Increasing
weakened if the N:P ratio of phytoplankton
Iron was relatively flexible.
deposition
Although the mechanisms that would
sustain Redfield’s envisaged homeostasis
Climate
Atmospheric of the marine N cycle are still unclear, past
CO2
biogechemical changes reconstructed from
marine sediments tend to support it. For
example, despite large-scale reorganizations
Figure 2 | Feedbacks governing the marine N cycle. Figure adapted with permission from ref. 5, © 2008, of the oceanic denitrification regimes across
Academic Press. the last transition from a glacial to an
interglacial climate state11, there appear to
be only minimal changes in the marine N
the activity of which “must tend to bring diazotrophic feedback depends on just how content, implying strong stabilizing feedbacks
the proportions of [nitrate and phosphate] much their activity is slowed by a lack of in the marine N cycle — unless, of course,
toward the ratio in which these substances iron. This is still intensely debated, leaving iron limitation during the deglaciation
occur in the bacterial protoplasm.” This the strength and efficiency of this feedback weakened the N-fixation feedback and
statement was a leap into the unknown: highly uncertain. reduced the glacial inventory of bioavailable
in 1934 when Redfield formulated this Since Redfield’s seminal contributions, N, as one recent analysis4 indicates.
hypothesis, no N-fixing organism had been marine denitrification has been ascribed
observed yet in the ocean. Now, a large a similar role in the stabilization of the Homeostasis in the Anthropocene
number of organisms capable of marine marine N content. Denitrifying bacteria Redfield’s earliest papers pictured an ocean
N-fixation (diazotrophs) have been and are consume nitrate while oxidizing organic in steady state, an assumption befitting the
continuing to be identified6, and marine matter when oxygen becomes depleted in long-term consistency thought to be inherent
N-fixation is recognized as the primary either the oxygen minimum zones (OMZ)10 in deep-ocean nutrient data (and the short
source of new bioavailable nitrogen entering or in marine sediments. The denitrification time series available then). His early work
the ocean5. feedbacks in both these locations arise could scarcely have anticipated the extent
The feedback in Redfield’s hypothesis because of a close link between the N loss of the changes in the N cycle inferred from
holds that N-fixing microbes occur in a by denitrifying bacteria and the N limitation the geologic record, much less the ones
well-identified niche of waters containing of phytoplankton (Fig. 2). This feedback can now being observed in the ‘Anthropocene’:
low nitrate but sufficient phosphate. This operate relatively quickly. The upwelling of a multitude of drivers has already begun
hypothesis is borne out by the modern N-deficient water immediately above the to perturb the marine N cycle, and given
distribution of diazotrophic organisms7. The OMZ or sediments limits phytoplankton current trends, is likely to cause even larger
rate of N fixation8 in various regions of the growth and reduces the amount of organic changes in the future (see also Fig. 2).
world’s oceans also matches that predicted matter that sinks into the OMZ or onto Climate warming is altering the
by this stabilizing feedback. It stands to the sediments. This limits the amount of oxygenation of the ocean’s interior 12;
reason that if the ocean were to begin losing nitrate required to consume the organic the OMZs that host most of the world’s
nitrogen, the extent of the diazotrophic matter, allowing nitrate concentrations denitrification are intrinsically sensitive
niches would greatly expand, permitting to rise. The feedback can also occur more to small perturbations of oxygen
the N fixers to slowly reconstitute the slowly through processes involving the concentrations. Changes in land use and
bioavailable N content (Fig. 2). basin-scale oxygen concentration. In the the hydrological cycle are predicted to
One trait could greatly curtail the ability case of an N excess, the high productivity of mobilize and solubilize the iron in dust,
of diazotrophic plankton to exploit their phytoplankton and subsequent high export enhancing its supply over large swathes of
ecological niche and stabilize the marine of organic matter would cause an increase the sea surface and potentially lessening iron
N cycle: they have a high demand for iron9, in thermocline oxygen consumption, limitation in several key areas. In addition,
a metal that is scarce in seawater. Whether resulting in an expansion of the OMZ and ocean acidification has been shown to alter
iron represents the Achilles heel of the enhanced denitrification. the rates of N fixation substantially. But the

854 NATURE GEOSCIENCE | VOL 7 | DECEMBER 2014 | www.nature.com/naturegeoscience

© 2014 Macmillan Publishers Limited. All rights reserved

 commentary

most direct effect of human activity on the whether they do so through phenotypic Nicolas Gruber is in the Environmental
oceanic N cycle is the massive application or genotypic changes. Clear latitudinal Physics group, Institute of Biogeochemistry and
of fertilizers full of bioavailable N, much trends in the N:P ratio of phytoplankton Pollutant Dynamics, ETH Zürich, 8092 Zürich,
of which makes its way to the ocean communities have been found14,15. It Switzerland. Curtis A. Deutsch is at the School of
either via rivers or through long-range remains to be seen whether the shifting Oceanography, University of Washington, Seattle,
atmospheric transport 13. boundaries of major ocean biomes can Washington 98195, USA.
Currently, we can only speculate alter the large-scale patterns of plankton e-mail: [email protected]
about how these perturbations, and their N:P ratios, and how that would modify the
interactions, will alter the marine nitrogen stabilizing feedbacks. References
cycle and affect its homeostasis. Given Redfield’s pioneering view of the 1. Redfield, A. C. in James Johnston Memorial Volume
(ed. Daniel, R. J.) 176–192 (Univ. Press of Liverpool, 1934).
that most stabilizing feedbacks operate ocean as a system capable of homeostatic 2. Redfield, A. C. Am. Sci. 46, 205–221 (1958).
on timescales of decades and longer, it is regulation helped pave the way for the 3. Deutsch, C., Sigman, D. M., Thunell, R. C., Meckler, A. N. &
likely that we will see widespread temporal broader and now commonplace recognition Haug, G. H. Glob. Biogeochem. Cycles 18, GB4012 (2004).
imbalances in the marine nitrogen cycle. that life alters its environment at a global 4. Eugster, O., Gruber, N., Deutsch, C., Jaccard, S. L. & Payne, M. R.
Paleoceanography 28, 116–129 (2013).
Indeed, the available time series from scale. Many of his insights have endured 5. Gruber, N. in Nitrogen in the Marine Environment 2nd edn
instrumental records and sedimentary the ongoing confrontation with new data (eds Capone, D. G., Bronk, D. A., Mulholland, M. R. &
records spanning the past 200 years suggest and refined explanatory models. Yet he Carpenter, E. J.) 1–43 (Academic, 2008).
6. Zehr, J. P. & Kudela, R. M. Annu. Rev. Mar. Sci.
that changes in major biological fluxes was keenly aware of the limitations of his 3, 197–225 (2011).
can be large, although their relationship explanations: “Whatever its explanation, 7. Luo, Y.-W., Lima, I. D., Karl, D. M., Deutsch, C. A. & Doney, S. C.
to forcing agents and their net effect on the correspondence between the quantities Biogeosciences 11, 691–708 (2014).
8. Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. &
the overall N budget remain uncertain. It of biologically available nitrogen and Dunne, J. P. Nature 445, 163–167 (2007).
is also unclear to what degree changes in phosphorus in the sea and the proportions 9. Falkowski, P. G. Nature 387, 272–275 (1997).
the N cycle will affect the working of the in which they are utilized by the plankton 10. Codispoti, L. A. in Productivity of the Ocean: Present and
Past (eds Berger, W. H., Smetacek, V. S. & Wefer, G.) 377–394
other biogeochemical cycles in the ocean, is a phenomenon of great interest”. In light (Wiley, 1989).
in particular the biological carbon pump. of the pace of basic discoveries and the 11. Galbraith, E. D. et al. Nature Geosci. 6, 579–584 (2013).
Perhaps the largest uncertainty stems growing imprint of humankind on the 12. Keeling, R. F., Kortzinger, A. & Gruber, N. Annu. Rev. Mar. Sci.
2, 199–229 (2010).
from the question of whether and how fast ocean, our understanding of the oceanic 13. Gruber, N. & Galloway, J. N. Nature 451, 293–296 (2008).
organisms and ecosystems can adapt to the N:P ratio is likely to continue to encounter 14. Martiny, A. C. et al. Nature Geosci. 6, 279–283 (2013).
changed environmental conditions, and new surprises. ❐ 15. Weber, T. S. & Deutsch, C. Nature 467, 550–554 (2010).

The elements of marine life

Noah J. Planavsky
Today, the ratio of carbon to nitrogen and phosphorus in marine organic matter is relatively constant. But
this ratio probably varied during the Earth’s history as a consequence of changes in the phytoplankton
community and ocean oxygen levels.

F
ew observations have had as nutrient cycling. But given that the oceans C:N:P ratios. For instance, the N:P ratios of
profound an impact on biological have been subject to major biological and modern marine primary producers span an
and chemical oceanography as geochemical evolutionary events throughout order of magnitude4–6.
Alfred Redfield’s recognition that the the geologic record, we should question A shift in the ecology of primary
elemental stoichiometry of most marine life whether C:N:P ratios have really remained producers could therefore result in a non-
is nearly constant 1. As originally noted by invariant through the Earth’s history 2. Redfield ocean. In the modern ocean,
Redfield in the 1930s — and subsequently The Redfield ratio may arise from different marine biomes have disparate
confirmed by thousands and thousands of the physiology of phytoplankton3, but C:N:P ratios. Therefore, as the balance of
measurements — there is a strong linear this notion is based largely on empirical biomes changes, so too could the mean
correlation (with a slope of 16:1) between observations4. The covariation of dissolved elemental stoichiometry of marine life.
dissolved nitrate and phosphate levels nitrate and phosphate in modern marine There have been several well-documented
in the modern oceans. This correlation settings, from which the Redfield ratio transitions in the phytoplankton
between nitrate and phosphate gave rise has been inferred, may be based on composition of the ocean throughout
to the concept that marine life had a biological feedbacks but is also strongly the Earth’s history 7,8. The most recent
fixed carbon:nitrogen:phosphorus ratio dependent on the mixing of water masses was, perhaps, the evolution of diatoms
(C:N:P = 106:16:1), which subsequently with disparate N:P ratios4. Furthermore, around 200 million years ago. Diatoms
became known as the Redfield ratio. This although the Redfield ratio seems to be are ubiquitous in modern ecosystems, but
ratio has become a cornerstone in our a global phenomenon, different groups only reached their present abundance in
understanding of marine carbon and of phytoplankton have widely varying the past 20 million years. Regions in which

NATURE GEOSCIENCE | VOL 7 | DECEMBER 2014 | www.nature.com/naturegeoscience 855

© 2014 Macmillan Publishers Limited. All rights reserved