Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats
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Global Change Biology (2001) 7, 849±882
FORUM
Primary productivity of planet earth: biological
determinants and physical constraints in terrestrial and
aquatic habitats
RICHARD J. GEIDER,1 EVAN H. DELUCIA,2 PAUL G. FALKOWSKI,3
ADRIEN C. FINZI,4 J. PHILIP GRIME,5 JOHN GRACE,6 TODD M. KANA,7
JULIE LA ROCHE,8 STEPHEN P. LONG,2,9 BRUCE A. OSBORNE,10
TREVOR PLATT,11 I. COLIN PRENTICE,12 JOHN A. RAVEN,13
WILLIAM H. SCHLESINGER,14 VICTOR SMETACEK,15 VENETIA STUART,16
SHUBHA SATHYENDRANATH,11,16 RICHARD B. THOMAS,17
TOM C. VOGELMANN,18 PETER WILLIAMS,19 F. IAN WOODWARD5
1
Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK, 2Department of Plant Biology, University of
Illinois, Urbana, IL 61801, USA, 3Institute of Marine and Coastal Sciences and Department of Geology, Rutgers University, 71
Dudley Road, New Brunswick, New Jersey 08901, USA, 4Biology Department, Boston University, Boston, MA 02215, USA,
5
Department of Animal and Plant Sciences, The University of Shef®eld, Shef®eld S10 2TN, UK, 6Institute of Ecology and
Resource Management, The University of Edinburgh, Edinburgh EH9 3JU, UK, 7Horn Point Laboratory, University of
Maryland, PO Box 775, Cambridge MD 21613, USA, 8Institut fuÈr Meereskunde, DuÈstenbrooker Weg 20, Kiel 24105, Germany,
9
Department of Crop Science, University of Illinois, Urbana, IL 61801, USA, 10Botany Department, University College Dublin,
Bel®eld, Dublin 4, Ireland, 11Bedford Institute of Oceanography, Dartmouth, Nova Scotia B2Y 4A2, Canada, 12Max Plank
Insttitute for Biogeochemistry, Carl-Zeiss-Promenade 10, Jena D-07743, Germany, 13Department of Biological Sciences,
University of Dundee, Dundee DD1 4HN, UK, 14Department of Botany, Duke University, Durham, NC 27708, USA, 15Alfred
Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany, 16Dalhousie University,
Halifax, Nova Scotia, B3H 4J1, Canada, 17Department of Biology, West Virginia University, Morgantown, WV 26506, USA,
18
Botany Department, University of Wyoming, Laramie, WY 82071, USA, 19School of Ocean Sciences, University of Wales,
Bangor, Menai Bridge, Gywnedd, PP59 5EY, UK
Keywords: carbon cycle, climate change, photosynthesis, net primary productivity (NPP)
Introduction to the forum Understanding the controls on primary productivity of
the biosphere is one of the fundamental aims of global
The habitability of our planet depends on interlocking
change research. This forum addresses several key
climate and biogeochemical systems. Living organisms
questions regarding the role of the biota in the carbon
have played key roles in the evolution of these systems.
cycle. It begins with Ian Woodward's overview of the
Now man is perturbing the climate/biogeochemical
global carbon cycle and concludes with John Raven's
systems at an unprecedented pace. In particular, the
historical perspective of the negative feedbacks that
global carbon cycle is being forced directly by changes in
in¯uenced the evolution of embryophytes in the
carbon ¯uxes (e.g. fossil fuel burning and deforestation/
Devonian. In between, the forum focuses on the process
reforestation), and indirectly through changes in atmos-
of net primary production (NPP).
pheric chemistry (e.g. stratospheric ozone depletion and Despite differences in the structures of planktonic and
increases of green house gases). Nutrient cycles are also terrestrial ecosystems, notably of response of biomass to
being perturbed, with implications for the carbon cycle. It environmental change, there are common problems
is imperative that we learn how these changing condi- affecting both terrestrial and oceanic studies of NPP.
tions will in¯uence terrestrial and oceanic photosynthesis This has resulted in the parallel evolution of approaches
and biogeochemistry. to NPP research in very different milieux involving
advances in the technology required to study interacting
processes that cut across a range of space and time scales
Correspondence: Richard J Geider, Department of Biological
Sciences, University of Essex, Colchester CO4 3SQ, UK, (Table 1). The problems include estimating NPP of whole
tel + 44(0)1206-873312, fax + 44(0)1206±873416, e-mail geider@- plants and phytoplankton populations from gas
essex.ac.uk exchange measurements on leaves or subpopulations,
ã 2001 Blackwell Science Ltd 849850 R . J . G E I D E R et al.
Table 1 A chronology of technological innovations in NPP research
Terrestrial Marine
1940s
Lindeman establishes approaches based on NPP estimated from O2 light-dark bottle
energetic considerations. technique.
Riley develops dynamic food-chain models of
phytoplankton production.
1950s
A range of methods based on various biomass NPP estimated from in situ diel O2 changes.
measures and energy ef®ciency estimates
introduced. Spectrophotometric method for measuring
chlorophyll developed.
Steemann±Nielsen introduces 14C technique to
estimate NPP.
Models of water-column NPP developed.
1960s
International Biological Programme (IBP) develops Introduction of use of 15N labelled
standardized techniques for NPP estimation of compounds to estimate new and
major terrestrial biomes. regenerated production.
Development of ¯uorometric method for
measuring chlorophyll.
1970s
Micrometeorological method applied to crop and In situ ¯uorometry applied to systematic
grassland systems. mapping of the subsurface chlorophyll a
Errors resulting from biomass turnover in maximum and frontal features.
estimates of NPP demonstrated. Independent estimates of NPP and export
Problems of estimating below-ground component production lead to questioning of the accuracy of the
14
NPP with any precision highlighted. C technique.
Concepts of light interception and conversion
ef®ciencies introduced.
1980s
Eddy covariance technique developed. High precision TCO2 and O2 determinations
Underestimation of NPP from IBP methods allowed extension of in situ diel techniques to
demonstrated. oligotrophic regions.
Satellite remote sensing of leaf area and Satellite remote sensing of pigments introduced
interception ef®ciency developed (NDVI). and bio-optical algorithms for obtaining
Rhizotrons and computerized image analysis for productivity developed.
estimating below-ground NPP. Questions about 14C technique largely resolved.
Effective models for scaling from the Emergence of coupled physical-biological modelling.
photosynthetic process to canopies developed. Trace element clean techniques allow iron-
Mass isotope analysis allows separation of C4 limitation to be demonstrated in bottles.
and C3 components. HPLC technique for measuring phytoplankton
pigments perfected.
1990s
Long-term eddy ¯ux networks developed. Fast Repetition Rate ¯uorescence technique
Links to routine satellite monitoring of regional NDVI. introduced for in situ estimation of
Chlorophyll ¯uorescence and absorption photosynthetic ef®ciency.
spectroscopic methods for remote sensing of Iron limitation demonstrated unambiguously
photosynthetic conversion ef®ciency attempted. during Lagrangian studies involving water mass
labelling with SF6.
Widespread application of analytical ¯ow
cytometry to phytoplankton populations.
2000+
Major breakthroughs needed: Major breakthroughs needed:
Plant respiration models of the detail available for Remote sensing of photosynthetic ef®ciency
photosynthesis together with resolution of the to complement remote sensing of pigments
direct effects of rising CO2. and light attenuation.
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882NPP AND CLIMATE CHANGE 851
Table 1 (continued)
Terrestrial Marine
Below ground NPP remains poorly Extend remote sensing of pigments and
known and a major weakness in ground-truthing. productivity to near shore waters with high
sediment and dissolved organic matter.
Effective method of remote sensing of conversion Establish the contribution of nitrogen
ef®ciency to complement satellite remote sensing ®xation to new production
of NDVI. Increase biological and spatial resolution of
global or basin scale physical-biological-
geochemical models to link biological production to
the ¯ows of carbon between the atmosphere
and deep ocean.
Table 2 Scales of variability and experimental approaches in NPP research
Terrestrial Systems Planktonic Systems
Scale Approach Scale Approach
Cell/tissue/leaf Leaf gas exchange Single cell In vitro incubations
Whole plant Physiological models whole
plant gas exchange
Canopy Free air measurements Water column In situ measurements
Landscape Free air measurements Water mass Water parcel marking
with SF6 (25 km2) and
in situ measurements
Biome Satellite remote sensing Biogeochemical province Satellite remote sensing
of vegetation and of chlorophyll and
extrapolation to NPP extrapolation to NPP
Biosphere Biogeochemical models Biogeochemical models
accounting for heterotrophic metabolism in gas exchange (Longhurst et al. 1995; Field et al. 1998). Despite the
measurements, extrapolating from small scales to global consistency of these estimates, their accuracy is still an
NPP (Table 2), developing mechanistic models of NPP open question. John Grace notes, based on free-air
and biomass accumulation, and relating NPP to the techniques, that we may ®nd that the terrestrial bio-
cycling of other elements. Although small-scale meas- sphere is 20±50% more productive than hitherto sup-
urements will continue to be a staple tool in investiga- posed. There also remains dif®culty in reconciling
tions of NPP, use of open system measurements systems biogeochemical evidence of high productivity on the
have necessarily come to the fore. These include free-air annual and longer time scales with measurements of
CO2 exchange in terrestrial systems and water mass marine NPP made on physiological time scales (Jenkins
tracking in aquatic systems. Deliberate experimental & Goldman 1985).
manipulations will increasingly supplement correlative Our current understanding of global NPP is based on
studies to derive insights into environmental regulation the extrapolation of local studies to the global scale (Field
of NPP and the feedback between plant productivity and et al. 1998). Satellite sensors provide measurements of
biogeochemical cycles. vegetation cover on land and chlorophyll a concentra-
The net primary production of planet earth has tions in the sea from which the rates of light absorption
recently been estimated to equal about 1017 g C year±1 are calculated. These are converted to estimates of NPP
(Field et al. 1998; Table 3). The recent estimate for using algorithms that describe the dependence of photo-
terrestrial production of 56 Pg C year±1 is remarkably synthesis on the rate of light absorption. These algo-
similar to Whittaker & Likens (1975) value of 59 Pg C rithms, and hence estimates of global NPP, depend
year±1. The estimates for oceanic production have con- critically on a data base of gas exchange measurements.
verged on values of around 40±50 Pg C year±1 As emphasized by Tom Vogelmann, an understanding of
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882852 R . J . G E I D E R et al.
Table 3 Annual and seasonal net primary production (NPP) of the major units of the biosphere. All values are in petagrams of
carbon (1 Pg = 1015 g) based on data and citations contained in Longhurst et al. (1995) and Field et al. (1998)
Marine NPP Terrestrial NPP
Trade Winds Domain (tropical and subtropical) 13.0 Tropical rainforests 17.8
Westerly Winds Domain (temperate) 16.3 Broadleaf deciduous forests 1.5
Polar Domain 6.4 Mixed Broadleaf and needleleaf forests 3.1
Coastal Domain 10.7 Needleleaf evergreen forests 3.1
Salt marshes, estuaries and macrophytes 1.2 Needleleaf deciduous forest 1.4
Coral Reefs 0.7 Savannas 16.8
Perennial grasslands 2.4
Broadleaf shrubs with bare soil 1.0
Tundra 0.8
Desert 0.5
Cultivation 8.0
Total 48.3 56.4
the fundamental determinants of photosynthesis The wedding of ecology with biogeochemistry pre-
within leaves will facilitate the scaling of photosynthesis sents a challenge to oceanographers and terrestrial
from the leaf to the whole plant. Similarly, an under- systems scientists. It is widely recognized that NPP
standing of the fundamentals of light absorption and cannot be isolated from other biogeochemical consider-
photosynthetic responses of phytoplankton cells will ations. Less widely recognized are the ecological inter-
facilitate scaling to water column NPP. Shubha actions that determine community structure and, in turn,
Sathyendranath, Trevor Platt and Venetia Stuart describe in¯uence NPP.
the dual role of phytoplankton absorption that in¯uences Bottom-up controls provide a link between NPP and
both the rate of light-limited photosynthesis and the biogeochemistry. There is a need to move from single
quantity and spectral quality of underwater light. Todd factor models, to multifactor models that recognize a
Kana describes the common mechanisms of acclimation multiplicity of controls. Julie La Roche describes the need
of the photosynthetic apparatus to multiple environmen- to establish a hierarchy of controls by N, P, Si and Fe for
tal factors that should facilitate extrapolation at the understanding oceanic primary productivity and selec-
global scale. tion of functional groups of phytoplankton. However,
There is still considerable uncertainty in the physical Victor Smetacek warns that plankton evolution is driven
and chemical factors and ecological interactions that by ef®cacy of defence systems rather than competitive-
limit NPP in both terrestrial and aquatic systems. ness of resource-acquisition mechanisms, and that bot-
Colin Prentice points out that major uncertainties and tom-up processes will be insuf®cient to describe
discrepancies among models when projected into plankton population dynamics.
different climates arise because basic theoretical issues Steve Long notes the need for mechanistic models
have not been resolved. It has become increasingly capable of predicting biological feedback to the carbon
evident in recent years that integration of investiga- cycle under atmospheric change. In contrast, Philip
tions from basic biochemistry and biophysics of Grime argues that models based on plant functional
photosynthesis to whole plant responses to regional types are more likely to lead to insights into the
and global studies are essential for developing a ecological responses of NPP to climate change than are
predictive understanding of NPP. Steve Long notes the more traditional plant growth models that have been
the potential for intensive studies of individual stands derived from agronomy. Evan DeLucia and colleagues
subjected to ®eld-scale manipulation of climate and conclude that NPP of young forests will increase as the
atmosphere to provide a way forward in the devel- level of CO2 in the atmosphere continues to rise, but that
opment of more mechanistic models of terrestrial NPP. the magnitude and duration of these increases are highly
Similarly, Lagrangian studies, in which parcels of uncertain. More needs to be learned about the modula-
water are marked with the tracer SF6 and subjected to tion of NPP and maximum biomass by the availability of
deliberate manipulation, such as addition of iron, are other resources.
providing a new and powerful tool for investigating On seasonal, annual and decadal time scales, the
plankton systems (Coale et al. 1996). dynamics of O2 and CO2 reservoirs provide a rich data
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882NPP AND CLIMATE CHANGE 853
set for validation of global carbon cycle models. ¯uxes to and from vegetation. The current situation is
However, these integrative measurements can only be that a poorly quanti®ed pre-industrial global carbon
interpreted within the context of models of the geo- cycle is being subjected to human forcing, directly
graphical distribution of sources and sinks. Colin through changes in carbon ¯uxes and pools and indir-
Prentice indicates the need to keep an open mind about ectly through changes in climate. In terms of anthro-
the structure of terrestrial carbon budget models and that pogenic concern there are two major questions regarding
the atmospheric observations and experimental evidence the global carbon cycle. How will the cycle respond in
should be critically evaluated in the light of alternative this non-equilibrium mode, in particular how will
theories. Paul Falkowski has a similar message regarding increasing concentrations of atmospheric CO2 in¯uence
marine systems. He warns that ocean primary product- terrestrial and oceanic photosynthesis and chemistry? In
ivity is unlikely to be in steady state on any time scale an era when mitigation strategies are on the international
and that the feedbacks between marine productivity and agenda, how effective and for how long will natural
the climate/biogeochemical cycle system are not easily carbon sinks absorb signi®cant fractions of anthropo-
predicted. genic carbon releases?
Predictive models of the responses of the interlinked
climate and biogeochemical systems to anthropogenic
forcing are essential for providing rational decisions on The oceanic sink
the use of fossil fuel and the potential for deliberate Most of the early ocean work was concerned with
manipulation of the carbon system to mitigate against de®ning environmental impacts on the solubility of
rising atmospheric CO2. However, at this stage in our CO2 in water ± the so-called solubility pump. The
understanding of planet earth, we lack predictive power effectiveness of the solubility pump at sequestering
and it is important that we recognize the limits of our anthropogenic releases of CO2 depends on ocean
knowledge. Whether the climate/biogeochemical sys-
temperature, vertical mixing and global circulation
tems will ever be wholly predictable is uncertain. What is
patterns (Falkowski et al. 2000). More recent work has
certain, however, is that avenues for fruitful research
also considered biological uptake of CO2 in the
continue to open up as technological opportunities and
oceans ± the biological pump. The biological pump
our knowledge-base expands.
describes the processes by which phytoplankton
absorb CO2 from the surface waters by photosynthesis.
The global carbon cycle (F. IAN WOODWARD) Following respiratory losses, dead organic matter and
commonly associated calcium carbonate descend from
The pool of carbon in the atmosphere and its monthly,
the photic ocean surface to the ocean interior, effect-
annual and decadal dynamics is the best-quanti®ed
ively locking carbon away from the atmosphere for
component of the global carbon cycle (Keeling &
extended periods. This pump has not generally been
Whorf, 2000). The terrestrial and oceanic carbon pools
considered important in absorbing further increases in
exchange primarily with the atmosphere, but none of the
anthropogenic CO2 because CO2 uptake by phyto-
individual pools or ¯uxes are known with great preci-
sion, due to their marked spatial variability and large plankton is primarily limited by the supply of nutri-
sizes. However, the net effect of large terrestrial and ents such as nitrogen, phosphorus and iron, and
oceanic source and sink ¯uxes on the atmospheric pool of increasing CO2 supply should have little impact
carbon can be determined from the trends in atmospheric (Heimann 1997). Future changes in ocean circulation
CO2 recorded since continuous monitoring was insti- patterns and strati®cation, in response to global
tuted in 1958 (Keeling & Whorf, 2000). Between 1991 and warming, will exert signi®cant impacts on the avail-
1997 only about 45% of industrial CO2 emissions accu- ability of nutrients and the effectiveness of the
mulated in the atmosphere (Battle et al. 2000), indicating biological pump. Sarmiento et al. (1998) suggest that
that the terrestrial and oceanic sinks must in¯uence the changes in the biology of the pump may be the most
atmospheric accumulation. There is also now an improv- critical component of the oceanic responses to future
ing capacity to differentiate between terrestrial and changes in climate and CO2. Unfortunately, for future
oceanic ¯uxes (e.g. Battle et al. 2000). These measure- projections, Sarmiento et al. (1998) conclude that the
ments show that the carbon cycle is out of equilibrium as response of the biological oceanic community to the climate
a result of human activities. Releases of carbon through change is dif®cult to predict on present understanding.
fossil fuel burning are quite well quanti®ed but the Perhaps the future approach may need to be closer to
impacts of deforestation on carbon release are less well that taken for terrestrial ecosystems, with a greater
characterized (Nepstad et al. 1999) and are not readily emphasis on carbon ¯ux physiology, nutrient
distinguishable, by atmospheric measurements, from exchange capacity and community dynamics.
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882854 R . J . G E I D E R et al.
The terrestrial sink capacity. However, there is evidence for a decline in this
capacity as the CO2 stimulation of productivity reaches
The turnover of marine phytoplankton is very rapid, on
saturation.
the order of a week, and so any increases in productivity,
through CO2 and nutrient enrichment, will have rather
little impact on standing stocks. This contrasts with the Uncertainty
decadal-scale turnover for trees, the dominant terrestrial
Estimates of oceanic and terrestrial sink capacities for
sinks and for which even small increases in productivity
carbon are currently quite uncertain but the best that can
could lead to substantial increases in carbon storage. The
be achieved to date comes from three major and largely
longevity and dynamics of trees, particularly through
independent methods of estimation. The three methods
natural and anthropogenic disturbances, are critical for
are, broadly, the inversion of time series of atmospheric
de®ning the terrestrial part of the global carbon cycle.
composition (e.g. CO2, O2 and d13C), in situ observations
There is abundant evidence that plants can increase their
and model simulations. No single technique is currently
photosynthetic capacity with CO2 enrichment. However
adequate for a full and accurate global picture of the
this response slows with increasing CO2 and, like the
spatial and temporal activities of the global carbon sinks.
phytoplankton, is also in¯uenced by the supply of other
The measurements of atmospheric composition are
nutrients, in particular nitrogen and phosphorus.
sparse, particularly over the terrestrial biosphere, and
Modelling (Cao & Woodward 1998) and experiment
sinks can only be estimated from measurements after the
(DeLucia et al. 1999) now indicate clearly that ecosystems
use of atmospheric transport models. In some cases maps
can increase their carbon sequestering capacity with CO2
of vegetation distribution are also required. This is
enrichment, but that the oft-vaunted impacts of pollutant
particularly so for the interpretation of d13C data,
N deposition are rather small (Nadelhoffer et al. 1999).
where the distribution of species with the C4 pathway
of photosynthesis is required. In situ observations of CO2
Absorbing anthropogenic releases of CO2 with climatic ¯uxes, or temporal changes in the sizes of carbon pools,
change are also sparse, particularly over the oceans and between
Increased oceanic sequestration of atmospheric CO2 as the tropics. In addition, observations on land need to
organic matter causes a transfer to the ocean interior. track impacts on CO2 ¯uxes of processes such as
Unfortunately, this also locks away the nutrients that disturbance, harvesting and changes in land use.
limit carbon sequestration. Projections of the future Finally, models have the problems of insuf®cient under-
climate indicate warming and an increase in precipita- standing of processes, of oversimpli®cation and of severe
tion, both of which will tend to increase strati®cation and limitations to adequate testing. Reducing these uncer-
reduce upwelling of nutrients. In addition, the supply of tainties will require improved interactions between these
wind-blown iron, a limiting marine nutrient, from the three approaches. This will involve the assimilation of
dry continents may be reduced with a wetter climate. In observations, such as from remote sensing, into models
combination, these features should decrease the capacity and the wider use of statistical techniques for investigat-
of the biological pump (Falkowski et al. 1998) to sequester ing model and data uncertainties. There is still some way
anthropogenic carbon. However, changes in oceanic to go before the uncertainties of the carbon cycle can be
circulation patterns and, in areas with increased precipi- minimized so that, for example, continental-scale sinks
tation, increased estuarine runoff with high concentra- can be identi®ed and quanti®ed with precision and
tions of nutrients, may partially compensate for this small-scale observations can converge with global-scale
reduced oceanic activity. model simulations.
Experimental observations on plants suggest that CO2
enrichment can stimulate the carbon sequestering cap- Light absorption as a determinant of primary
acity but warming, with no change in water supply will productivity in algae (SHUBHA SATHYENDRANATH,
tend to reduce this capacity. Models at the global scale TREVOR PLATT AND VENETIA STUART)
(e.g. Cao & Woodward 1998) indicate that global climate
model simulations of future climatic warming alone Variations in the optical characteristics of phytoplankton
would cause a global decrease in the terrestrial sink can in¯uence primary production in two ways. First,
capacity for sequestering carbon, with vegetation and they affect the rate of light transmission underwater, and
soils adding to the atmospheric pool of carbon. The hence the magnitude of photosynthetically active photon
inclusion of the direct effects of increasing atmospheric ¯ux density (I) at depth. Second, they determine the rate
CO2 with this warming reverses this trend, with vege- of light absorption by phytoplankton and hence the rate
tation and soils increasing their carbon sequestration of light-limited photosynthesis.
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882NPP AND CLIMATE CHANGE 855
Absorption and scattering by pure water, the coloured Thus, the light regime at depth may be spectrally
component of dissolved organic matter, and particulate unfavourable for absorption by pigments, and hence
material (which includes phytoplankton) determine the for photosynthesis (that is to say, the wavelength integral
rate of light attenuation with depth. When computing the of the product of aB(l) and I(l) may be small, even if I(l)
phytoplankton contribution to light attenuation, it is not is high at some wavelengths). This effect may be
important to distinguish between photosynthetic pig- mitigated if the phytoplankton are able to adapt
ments, degradation products, or photoprotective pig- chromatically to the light ®eld at depth by modifying
ments. What is required in this context is that the their pigment composition. The high amounts of divinyl
phytoplankton component account for all pigments, chlorophyll b relative to divinyl chlorophyll a that are
regardless of their role in photosynthesis. often found at depth in some marine prochlorophytes
The requirements are, however, quite different and far (Moore et al. 1998) may re¯ect, in part, an adaptation to
more stringent if one is interested in calculating the the spectral quality of the light ®eld.
amount of light that reaches the photosystems of All these considerations demonstrate that primary
phytoplankton at a particular depth. In this context, it production in the water column is strongly in¯uenced by
becomes important to distinguish between absorption the absorption characteristics of phytoplankton. This has
and scattering; between absorption by phytoplankton led to a considerable interest in understanding natural
and absorption by other components of the system; and variability in the optical properties of phytoplankton.
between absorption by photosynthetic pigments and
non-photosynthetic pigments (in which group one might
Absorption characteristics of phytoplankton in the
combine degradation products and photoprotective pig-
aquatic environment
ments). This is important, since the realized maximum
quantum yield of photosynthesis, fm, will depend on The biomass normalized absorption spectra, referred to
whether or not the absorption is by photosynthetic or as speci®c absorption spectra, can be treated as an
non-photosynthetic pigments. intrinsic property of phytoplankton at the time of
In addition to modifying the amount of light available measurement, independent of their concentration. All
at depth, phytoplankton in¯uence the spectral quality of measurements con®rm certain common traits in the
light at depth. The spectral dependence of photosyn- speci®c absorption spectra: they all have a broad
thesis ensures that primary production is a function of absorption maximum in the blue part of the spectrum
both the magnitude of the underwater radiant ¯ux (I) and a secondary absorption maximum in the red.
and the spectral quality of the light ®eld. There is ample However, measurements made in the last decade con-
evidence in the literature that these spectral effects, if ®rm that these spectra also exhibit a great deal of
ignored, can lead to signi®cant errors in computed variability around the common trends. Speci®cally, the
production (Kyewalyanga et al. 1992). magnitude of the speci®c absorption maximum in the
In all models of photosynthesis (PB) as a function of I, blue can vary over a factor of ®ve from one sample to
the initial slope, aB, and the available light, I, are coupled another, whereas the magnitude of the red peak can vary
together as a product. Note that the superscript B by a factor of two or more. The shapes of the peaks are
indicates normalization to the concentration of the main also variable.
phytoplankton pigment chlorophyll a (including divinyl Two factors are responsible for most of the observed
chlorophyll a), treating chlorophyll as an index of variations in phytoplankton absorption: changes in pig-
phytoplankton biomass (B). The proper way to incorpor- ment packaging and in pigment composition. Based on
ate fully the spectral dependence of photosynthesis is to theoretical considerations, it has long been demonstrated
replace the product aBI in non-spectral models by the that the absorption ef®ciency of pigments within cells
spectrally weighted integral òaB(l) I(l) dl, where l is the depends on how the pigments are packaged into discrete
wavelength, and the wavelength integral is taken over particles (Duysens 1956). When packaged into cells, the
the whole of the photosynthetically active range from 400 pigments tend to shade themselves, such that the total
to 700 nm. To introduce the biomass-normalized absorp- absorption by the pigments would be less than the
tion coef®cient (aB (l)), explicitly into the spectral model, absorption by the same pigments if they were distributed
we can write aB(l) = fm(l)aB (l) by which we recognize uniformly in solution. Using simple mathematical mod-
that aB, fm and aB are all wavelength dependent. els, Duysens (1956) showed that the `package effect'
An interesting consequence of the spectral dependence would increase (or the ef®ciency of absorption decrease)
in light absorption by phytoplankton is that the presence as a function of the spherical equivalent diameter of the
of phytoplankton in the surface layers of the ocean cells and the intracellular absorption coef®cient of the
contributes to the rapid depletion of ¯ux at those pigments. The decrease in ef®ciency of absorption due to
wavelengths favourable for phytoplankton absorption. packaging is most pronounced at the absorption maxima
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882856 R . J . G E I D E R et al.
and least pronounced at the absorption minima, such absorption in¯uences primary production through its
that the absorption spectra of pigments packaged into effect on the light-limited photosynthesis rate. Clearly,
particulate matter would appear ¯atter than those of the any study of aquatic primary production would be
same pigments in solution. grossly inadequate if it did not account correctly for this
The second well-known cause of variation in phyto- dual role of phytoplankton absorption. Efforts to do this
plankton speci®c absorption spectra is the varying properly are, however, confounded by the fact that there
in¯uence of absorption by pigments other than chloro- is a considerable variability in the absorption character-
phyll a (Sathyendranath et al. 1987). Phytoplankton are istics of phytoplankton in the natural environment, about
known to have pigment complements that are character- which we still have much to learn.
istic of their taxa. Nutritional status and photoacclima-
tion can superimpose additional variations. Normalizing
the absorption spectra to chlorophyll a eliminates vari- Photosynthetic mechanisms and biological
ations in the magnitude of the spectra due to variations constraints on primary productivity of algae
in the absolute quantity of chlorophyll a, but it does not (TODD M. KANA)
account for changes in the composition and relative An important issue in understanding the effects of global
concentrations of other pigments in the sample. change on NPP is partly one of understanding how the
Typically, phytoplankton cells in oligotrophic oceanic photosynthetic process is regulated by multiple environ-
waters are small and contain relatively high amounts of mental factors. Physiological regulation is under genetic
non-photosynthetic carotenoids, favouring high absorp- control at the level of gene transcription and translation
tion ef®ciencies (Bricaud et al. 1995). The speci®c for key photosynthetic components and under biochem-
absorption spectra tend to get ¯atter and lower in ical control at the level of enzyme activation and
magnitude towards eutrophic waters with large cells, excitation energy quenching (Falkowski & Raven 1997).
and towards greater depths where the concentration of Algae can provide important insights into physiological
photoprotective pigments is low. Adaptation of cells to regulation of photosynthesis, because they are evolutio-
low light tends to increase pigment concentration per narily diverse and exhibit broad variations in metabol-
cell, which will also tend to decrease the speci®c
ism, cell size, pigmentation, photosynthetic biochemistry
absorption with an increase in depth.
and biophysics, and habitat preference. Evolution of light
The last decade has seen considerable progress in our
harvesting components, in particular, has been extensive,
understanding of the factors that cause variations in
and the importance of spectral light absorption in the
phytoplankton absorption characteristics. However, we
ecology of algae, both within and between species, has
do not have enough information for quantitative para-
been documented (Kirk 1994). Moreover, there are
meterization of phytoplankton absorption in vivo, given
signi®cant differences among taxa in the regulation of
the pigment composition and particle size distribution. A
energy ¯ow through the photosynthetic apparatus.
major impediment is our imperfect knowledge of the
Despite this diversity, there exists a general pattern of
in vivo absorption characteristics of individual phyto-
regulation of light harvesting in response to light,
plankton pigments. Whereas the absorption and ¯uores-
temperature and nutrient availability.
cence characteristics of major phytoplankton pigments
Algae are able to alter key photosynthetic attributes
are well known, we still know very little about how these
that affect utilization of light energy. These include
characteristics may vary once the pigments are bound to
proteins and arranged in complex structures within cells. cellular light absorption, quantum ef®ciency and max-
In spite of encouraging beginnings (Hoepffner & imum photosynthetic capacity. A change in cellular
Sathyendranath 1991), we are still a long way from pigment concentration is an important mechanism that
establishing a de®nitive catalogue of the intracellular modi®es these attributes. Pigment concentrations
absorption characteristics of individual pigments. An respond to the immediate environment and are in¯u-
open question at the moment is whether the character- enced by a variety of factors, including irradiance,
istics of individual pigments vary signi®cantly between nutrient availability and temperature. Pigment concen-
different types of phytoplankton cells, due to differences trations are also affected by the `physiological state' of
in internal cell structure and organization. the cell, which depends on the cell's environmental
history (Geider et al. 1998). Given the number of factors
involved, it is not surprising that quantitative relation-
Concluding Remarks ships among pigment concentration, photosynthesis and
Phytoplankton absorption has a strong effect on the environmental variables are complex. Despite the com-
quantity and spectral quality of the underwater light plexity, broad patterns are consistent among taxa and
available for aquatic photosynthesis. Furthermore, across environmental factors and it is possible to de®ne
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882NPP AND CLIMATE CHANGE 857
unifying principals of photosynthetic regulation in ability of a cell to utilize photosynthetic reductant by
response to environmental cues. carbon assimilation and other reduction pathways that
affect Pmax.
Many of the quantitative differences among taxa can
Integration of light and material ¯uxes in algae
be accounted for by relating photosynthetic parameters
All algae are exposed to environments with ¯uctuations to relative growth rate (Kana & Gilbert 1987), or a related
of irradiance, temperature and nutrient availability at irradiance index such as the light-saturation parameter,
multiple frequencies. Despite this environmental com- IK, for growth. This works because there is a high degree
plexity, algal cells maintain a relatively constant elem- of conservation of material and energy utilization by
ental (e.g. C, N and P) composition. This is accomplished algae and cellular growth is related to the rate of
partly through mechanisms that modulate photosyn- photosynthetic carbon assimilation. In particular, under
thesis. These mechanisms operate at several dominant conditions of balanced growth Acell declines as I
frequencies including seconds (energy quenching), min- increases and the rate of cellular growth is given by
utes (xanthophyll cycle quenching) and hours to days G = I 3 Acell. This is accomplished through regulation of
(acclimation). pigment synthesis/degradation by the energy balance
Light, temperature and nutrient availability are ratio (e.g. I 3 Acell/Pmax) at subgenerational time-scales
important environmental factors that affect the concen- which translates to an energy (or material) balance at
tration of photosynthetic pigments in algal cells. Changes generational time-scales. This is consistent with negative
of cell pigment concentrations directly affect the ef®- feed-back regulation of cellular light harvesting.
ciency of light utilization and instantaneous photosyn- Signi®cantly, Acell in¯uences G, but it is also constrained
thesis rate, and are thus important in algal ecology. by the maximum value of G. The value of G is subject to a
Recent models integrate these factors and predict genetic constraint on the maximum cell division rate, but
acclimated pigment concentrations for an arbitrary can be modi®ed by nutrient-limitation or temperature.
environment (Kana et al. 1997; Geider et al. 1998). The This makes the photosynthetic apparatus as much a slave
various models incorporate an energy balance `signal' to the cell's ability to utilize energy as it is a provider of
that affects the rate of synthesis or degradation of that energy.
pigmentation. The energy balance is formulated as the
ratio of excitons entering the photosystems relative to
Photosynthetic pigment regulation
electrons removed from the photosystems (Kana et al.
1997). This signal may be sensed by the redox state of the Two schemes have been proposed for the regulation of
plastoquinone pool or some other redox sensitive the cellular pigment concentration according to the short-
component of the light reactions that in¯uences synthesis term energy balance of the photosynthetic apparatus.
or degradation of light harvesting compounds (Escoubas These are regulation of pigment synthesis rates by
et al. 1995). In the steady-state, the cellular pigment changes in the expression of genes controlling synthesis
concentration is poised at a level such that light energy of pigment-proteins (Escoubas et al. 1995) and regulation
input is in balance with the ¯ow of assimilate for growth. of pigment losses associated with photoinhibitory mech-
This condition illustrates the basic principal that regula- anisms (Kana et al. 1997). Considerable work needs to be
tion on long and short time scales tends towards a done to determine how these mechanisms interact in a
balanced energy ¯ow with respect to light absorbed and cell to modulate pigment concentrations under both
the capacity to utilize photosynthetic energy (Weis & steady-state and transient-state conditions and to deter-
Berry 1987). mine how other cellular processes modulate the energy
This balance can be parameterized as the ratio of balance. The nature of these energy and material balance
cellular light absorption to maximum assimilation rate, constraints on regulation of photosynthesis has made it
or I 3 Acell/Pmax, where I is irradiance impinging on the possible to broadly predict chlorophyll a : carbon ratios
cell, Acell is the fraction of incident irradiance absorbed, in natural environments (Taylor et al. 1997). This suggests
and Pmax is the maximum photosynthesis rate. Acell is that physiological regulation according to energy balance
determined by the acclimation response of the cell and is is more important than differences in a species' optical
roughly proportional to pigment concentration. Pmax is properties or metabolism at large ± ranging up to
determined largely by the physiological state of the cell, global ± scales. In some respects this is surprising,
which is affected by environmental factors such as given the diversity among taxa in cell size, temperature
temperature and nutrient availability. Quantitative dif- optima and the ef®ciency of nutrient uptake. As in the
ferences in these parameters among algae subjected to terrestrial realm it has increased the value of remote
different environments arise from differences in cell size sensing of light absorption (Table 1). The uncoupling of
and pigment complement which affect Acell and the these species-speci®c factors at the largest scales is likely
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882858 R . J . G E I D E R et al.
due to the large range in resource ratios found in nature. situ comparisons. The broad problem of the accuracy of
The in¯uence of resource availability on growth rate and the 14C measurement, which was perceived to be most
physiological acclimation may be overriding on a global acute in the vast oligotrophic parts of the ocean, was
scale. addressed by the US PRPOOS programme. Two papers
from that programme largely laid to rest the concerns
over in vitro methodology. Marra & Heinemann (1984)
Implications for global primary productivity
showed that potential contaminants from the incubation
In the context of global change and NPP, broad-scale vessels did not introduce a serious error when there was
patterns in steady-state physiological response are likely adequate attention to clean procedures. Williams &
to be predictable given a knowledge of changes in Purdie (1991) showed that in vitro techniques returned
resource availability. On the other hand, local transient similar rates of photosynthestic oxygen evolution as in
phenomena associated with higher frequency ¯uctu- situ techniques. Thus the earlier spectres were laid to rest
ations in resources, such as blooms, will be more dif®cult and the 14C data base was again recognized as a key
to predict. In environments that vary on the scale of resource for calibrating all other approaches for estimat-
physiological to multi-generational (hours to days), ing oceanic productivity.
species-speci®c responses are likely to be more import- The next development came with the application of in
ant. Cell mobility, nutrient storage, mixotrophy and situ ¯uorometry to measure the spatial distribution of
optical characteristics are amongst the factors that can phytoplankton. Over the mid 1970s and 1980s, ¯uorom-
determine short-term competitive success of speci®c eters were incorporated into systems that allowed con-
species in transient environments and affect the relation- tinuous sampling with high spatial resolution in the
ship between primary productivity and environmental vertical (approximately 1±10 m) and horizontal (approxi-
variables. The importance of biological diversity (the mately 10±100 m). This facilitated near real time, two-
opposite of biological constraints) is most important at dimensional mapping (e.g. Watson et al. 1991) and
this intermediate scale. Prediction at these scales is achieved three things. First, it showed the mesoscale
considerably more dif®cult than at narrower or broader (1±100 km) variability of phytoplankton distribution and
scales. This is a major contrast to the terrestrial environ- thus the limitations of in vitro methodology. Second, it
ment, where species' changes affecting NPP require made very clear the short-term in¯uence of physical
years to centuries. In the aquatic realm signi®cant shifts processes on plankton distribution. Third, it broadened
occur in days. horizons of the scale over which plankton processes need
to be measured. With the introduction of the fast
repetition rate ¯uorometer (Falkowski & Kolber 1993),
Assessing oceanic productivity (PETER WILLIAMS)
the ability to measure biomass has been supplemented
The in vitro 14C technique, introduced by Steemann± with the ability to measure photosynthetic ef®ciency.
Nielsen in 1952, provides the basis for our knowledge of This instrumentation is now being used in basin wide
oceanic primary productivity. The success of this studies. Mapping chlorophyll and productivity on these
approach can be measured by the development of global scales in a relatively inaccessible area such as the ocean
maps of oceanic productivity within a comparatively may be seen as a considerable technical and scienti®c
short period of the introduction of the technique. These advance in itself, but more important is that the scale of
maps, especially that of Koblents-Mishke et al. 1970), are the measurement matches those of satellite ocean obser-
remarkably accurate with respect to contemporary meas- vations, so providing the essential `ground truth'.
urements in describing distribution pattern of plankton The launching of the Nimbus 7 satellite in 1978 and the
productivity, although they are less accurate in describ- operation of the Coastal Zone Colour Scanner (CZCS)
ing the absolute rates. These successes, largely unchal- radiometer it carried until 1986 opened up the potential
lenged, and the comparative simplicity and sensitivity of to measure surface chlorophyll a concentrations on an
the approach meant that there was minimal pressure to ocean-wide scale and at a level of detail previously
develop new approaches. However, three developments unattainable (Feldman et al. 1989). It was quickly realized
in the post mid-1970s required that other approaches be that satellites could provide the necessary biomass data
examined. to model planktonic photosynthesis on an ocean-basin
The ®rst development was a concern over the accuracy scale. At its simplest, from knowledge of the in situ
of the in vitro 14C technique itself. Potential errors of the chlorophyll a concentration, the relationship between
14
C technique were assessed by cross calibrations against irradiance and photosynthesis, and the beam attenuation
high accuracy oxygen measurements. Potential errors coef®cient of the water column, the wherewithal exists to
associated with containment of the sample, i.e. contam- model plankton primary production. There are a number
ination and lack of turbulence, called for in vitro vs. in of technical problems that had to be surmounted. The
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882NPP AND CLIMATE CHANGE 859
CZCS radiometers had low precision, at best 35%; this in Atlantic. Jenkins (1988) in part resolved this by showing
part arises as only 10% of the satellite signal comes from that diapycnical transfer (e.g. across constant density
ocean colour ± the remaining 90% is associated with contours), using historical estimates of diffusion coef®-
processes occurring in the atmosphere and has to be cients, would fail by an order of magnitude to account
independently assessed and subtracted from the `chloro- for the rate of nitrate input needed to sustain net
phyll a signal'. Perhaps more fundamental, satellite ecosystem production. He also showed that the rates of
observations only return information on the upper 10± mixing could account for the required rate of nitrate
20 m of the ocean which represents only the upper 20% input using the distribution of 3H in the upper oceans.
of the photic zone. This exacerbates the problem of However, the physical mechanism driving the process is
estimating primary production as chlorophyll a distribu- unresolved. Jenkins (1988) suggested that it was due to
tions are neither constant nor monotonic, especially in isopycnical mixing (e.g. along constant density surfaces),
open ocean waters. There is often an intermediate deep but as things stand neither this nor any other physical
chlorophyll a maximum, characteristically between the mechanism has general acceptance.
10% and 1% light levels that occur at depths of 25±100 m. In conclusion, ocean productivity studies have made a
Platt et al. (1995) discussed the strategies for determin- remarkable and almost seamless transition from in vitro
ing photosynthetic rates from satellite observations and measurement of carbon ®xation in bottles to whole ocean
the problems associated with the distribution of chloro- productivity calculations based on satellite observations.
phyll a within the water column. Their solution was to Thus, a sound and singularly consistent pattern of
use the rationalization of Longhurst et al. (1995) that oceanic productivity has been attained. However, the
separated the oceans into four primary ecological physical and chemical controls on the process remain
domains (Table 3) and some 56 secondary ones. Within unclear.
these ecological provinces it was possible to use general-
ized parameters to describe the photosynthesis vs.
Aquatic primary productivity: the ultimate
irradiance (PI) curve and the distribution of chlorophyll
limiting nutrient, biogeochemical cycles and
a with depth. Given this, it was possible to produce
phytoplankton species dominance (JULIE LA
global maps of annual planktonic production (Longhurst
ROCHE)
et al. 1995). Field et al. (1998) used a simpler approach to
modelling marine production by using the data base of In the last decade, oceanographers have gained signi®-
14
C observations to determine the light utilization cant insight into the conditions and geographical loca-
ef®ciency of photosynthesis. It is signi®cant to note that tions that are associated with P, N, Si or Fe limitation of
although the Field et al. (1998) approach differed in detail primary productivity. However, we have not reached a
from that of Longhurst et al. (1995), the two approaches consensus regarding the nutrient that is most important
produce estimates for total annual oceanic productivity in limiting aquatic primary productivity. There has been
within 5% of one another. This, in all probability, is a long-standing debate regarding which nutrient, N or P,
greater than our ability to interpret the 14C ®eld obser- ultimately limits marine primary productivity. Despite
vations (Williams 1993). As such, these two papers must accumulated biological evidence that nitrogen limits
be seen to represent the completion of a major chapter ± phytoplankton productivity over the largest area of the
if not the major chapter ± on the estimation of oceanic world's ocean surface waters (Falkowski et al. 1998),
productivity. geochemists continue to argue, on theoretical grounds,
The above approaches assume that planktonic photo- that phosphorus must be the ultimate limiting nutrient,
synthesis is some function of four properties: these are globally and on geological time scales (Tyrrell 1999).
the local irradiance, chlorophyll a concentration, quan- The cycling of N is much more complex than that of P,
tum yield and local inorganic nutrient concentration. with signi®cant biologically mediated exchanges
Generally, the fourth factor may be contained within the between the atmosphere and the oceans, in the form of
quantum yield or observed photosynthesis±irradiance dinitrogen ®xation and denitri®cation. Nitrogen has a
relationship. very large atmospheric reservoir, in the form of N2 gas,
There remain major questions surrounding the control which in theory can be ®xed into reactive nitrogen by
of production by the inorganic environment of the open diazotrophs. Proponents of P limitation argue that any
oceans. Regardless of whether nitrogen or phosphorous imbalance between reactive N and P, due to low ®xed
controls production, where inorganic nutrients are nitrogen input to the ocean or increased denitri®cation,
clearly limiting there are dif®culties in reconciling will be rapidly counterbalanced by increased N2 ®xation.
calculations of nutrient input due to physical processes Experimental evidence and ®eld data suggest that this
with the estimated or measured rates of new production. may be the case for terrestrial habitats (Chadwick et al.
The problem is particularly acute for the subtropical 1999). In fact, there is overwhelming evidence supporting
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882860 R . J . G E I D E R et al.
P-limitation of primary production in most freshwater stimulates nitrogen ®xation (Paerl et al. 1994). While the
ecosystems. In contrast, there is little support for P- effect of Fe-limitation on diazotrophy may simply be
limitation in marine ecosystems. With a few exceptions, manifested by an overall decrease in growth rate, it is
nutrient addition bioassays and the distribution of N : P almost certainly a dynamic response as a function of Fe
ratios over the major oceanic basins, coastal areas and concentration.
estuaries demonstrate that N, and not P, stimulates Recent work has demonstrated that we know very
primary productivity (Falkowski et al. 1998). Until little about iron cycling, bioavailability and the physio-
recently, there have been relatively few new arguments logical effects of Fe-limitation on phytoplankton. The
to reconcile these opposite views. predominance of Fe as a cofactor in the nitrate assimi-
The oceanographic community has recently come to lation enzymes makes an obvious case for an interaction
terms with the crucial role that Fe availability plays in between nitrogen assimilation and Fe limitation in
some marine ecosystems (Coale et al. 1996). The basic phytoplankton. Despite this theoretical prediction, there
®ndings of the in situ Fe-enrichment studies are so are relatively few studies that convincingly demonstrate
convincing that most scientists agree that the case for Fe- a preference for NH4+ relative to NO3± in Fe-limited
limitation in certain high nutrient, low chlorophyll phytoplankton. In contrast, a link has been recently
regions has been established beyond reasonable doubt. uncovered between N, Fe and Si. The decrease in
More controversially, Behrenfeld & Kolber (1999) pro- nitrogen uptake in Fe-limited diatoms leads to an
vide evidence that iron limits primary productivity in increase in the Si : N uptake ratio of the cells (Hutchins
large areas of the low-nutrient oligotrophic Paci®c & Bruland 1999). The ultimate consequence is that Fe-
Ocean. This has revitalized the debate of N- vs. P- limited diatoms are heavily silici®ed and therefore sink
limitation. It has been suggested that low Fe availability faster than their iron-replete counterparts. This unex-
in seawater, prevalent since the rise of oxygen in the pected ®nding has far reaching implications for the
atmosphere approximately 2 billion years ago, has oceanic carbon cycle and for estimates of palaeoproduc-
greatly restricted oceanic nitrogen ®xation throughout tivity that use biogenic opal as a proxy. In a new liaison
geological times via the prevention of a major radiation with the nitrogen cycle, Hutchins et al. (1999) found that
in the diazotrophic branch of marine cyanobacteria and Fe bound to dissolved porphyrins and linear tetrapyr-
in the present via limitation of nitrogenase synthesis, an roles, cytochromes and haem proteins can be utilized
enzyme extremely rich in Fe (Falkowski 1997). preferentially by eukaryotic phytoplankton.
Tyrrell (1999) has recently countered, using a parsi- Tetrapyrroles, the building blocks of photosynthetic
monious model of N and P biogeochemical cycles, that pigments, have been recently identi®ed as a low abun-
phosphate is the ultimate limiting nutrient. In this model, dance but signi®cant component of the oceanic dissolved
phosphate controls the standing stock of nitrogen and the organic nitrogen (DON) pool (McCarthy et al. 1997).
observed oceanic N : P ratio, without the need to invoke Tetrapyrrole-like molecules are among the most stable
a signi®cant role for Fe. This is achieved in his model by organic nitrogen forms and some of the most highly
the assumption that dinitrogen ®xation is inversely preserved organic molecules in the marine environ-
related to the availability of ®xed nitrogen. This assump- ments. As strong Fe-ligands, these molecules could
tion is well supported by molecular biological studies signi®cantly affect the residence time of bioavailabale
demonstrating the repression of nitrogenase gene expres- Fe in the ocean (Hutchins et al. 1999). These new ®ndings
sion by ®xed nitrogen species in a multitude of suggest that we are not yet in a position to quantitatively
diazotrophs (Zhang et al. 1997). Other factors that can model the impact of Fe on primary production relative to
affect nitrogen ®xation are lumped in an overall reduc- that of P and N.
tion of the maximum growth rate of diazotrophs rather The search for the ultimate limiting nutrient may be
than incorporated as dynamic components of the model. misleading because the relative importance of the well-
This gives non-diazotrophs a competitive advantage known biolimiting nutrients N, P, Fe and Si may be on
when ®xed nitrogen is abundant. However, the assump- the selection of different functional groups of phyto-
tion that the sole dynamic control of nitrogenase lies in plankton. It is well known that primary production by
the relative abundance of nitrogen and phosphorus may various functional groups of phytoplankton and at
not be justi®ed. Speci®cally, given the large Fe require- speci®c locations can have very different impacts on
ment of nitrogenase, it seems logical that the control by the oceanic carbon cycle and on the interaction between
Fe of the synthesis of functional nitrogenase will tend to ocean and atmosphere. For example, Si is an essential
override the control exerted by ®xed nitrogen. Very little nutrient only for diatoms. However, Si may still work as
is known about the effect of Fe availability on the growth a key determinant in the global C-cycle because of the
of diazotrophs in general, and on the nitrogen ®xation important role played by diatoms in C-¯uxes to deep
pathway in particular, but there are reports that iron water. Like Fe, low Si concentrations have recently been
ã 2001 Blackwell Science Ltd, Global Change Biology, 7, 849±882You can also read
