Marine Ecology Progress Series 425:281

Vol. 425: 281–296, 2011 MARINE ECOLOGY PROGRESS SERIES Published March 14 doi: 10.3354/meps08882 Mar Ecol Prog Ser

OPENPEN ACCESSCCESS

REVIEW

Contrasting micro- and macro-nutrient nourishment of the ocean

Ian S. F. Jones*

Ocean Technology Group, University of Sydney, Sydney, New South Wales 2006, Australia

ABSTRACT: There have been suggestions that an increase in the productivity of the ocean would store more carbon in the ocean organic carbon cycle, as well as enhancing the higher trophic levels of the marine food web. Proposals have included fertilisation of regions low in one or more of nitrogen, phosphorus or iron, the latter being termed a micronutrient. Iron is available from mining, phosphorus from mining or artificially induced upwelling, and the provision of nitrogen involves using either cyanobacteria, the Haber-Bosch process or artificially induced upwelling. All these fertilisation methods can be effective in locally increasing new primary production, but the global impact varies because of iron scavenging, nutrient stealing or the role of regenerative primary production. Exami- nation of these concepts leads to the conclusion that macronutrient nourishment supplied by the Haber-Bosch process is an attractive approach for slowing climate change and increasing marine productivity. The carbon storage capacity of nitrogen fertilisation appears to be limited by the supply of phosphorus to support additional new primary production.

KEY WORDS: Climate change · Ocean carbon cycle · Ocean nourishment · Primary production

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INTRODUCTION upper ocean, phytoplankton captures carbon dioxide and converts it to organic carbon, in a partial analogy If the primary production of the ocean were to be in- of trees. Turbulent fluxes of carbon dioxide between creased as mankind has enhanced the primary produc- the ocean and the atmosphere resupply the inorganic tivity of agricultural lands, there could be benefits for carbon. Due to senescence and predation of the plank- both climate management and marine protein produc- tonic biomass, such carbon sinks to the deep ocean. If tion according to some scientists. Phytoplankton, the this process can be enhanced, carbon dioxide from the dominant component of marine new primary production, atmosphere could be stored in the deep-ocean organic takes carbon from the surface ocean to create organic carbon cycle, mitigating the threat of rapid climate material. This provides energy for higher trophic levels change. Concern about climate change sparked the in the marine food web and also produces a rain of car- Royal Society of London review of global-scale actions bon to the deep ocean, where it is isolated from the at- available to manage climate change (Shepherd 2009). mosphere. A fraction of the carbon falls to the sea floor. The review considered ocean fertilisation as an exam- Primary production on the land is often limited by ple of carbon dioxide removal from the atmosphere. the supply of nutrients and this limitation is relieved by The risks from climate change and the need for more the addition of fertiliser. Over 100 Mt (108 t) of nitrogen protein as the human population rises have prompted fertiliser is delivered to the land worldwide each year calls to increase the primary production of the world’s in order to increase the primary production, and some oceans. In this review, I will focus on fertilisation by of this fertiliser reaches the ocean as runoff. In the any of 3 nutrients: nitrogen, phosphorus and iron. The

*Email: [email protected] © Inter-Research 2011 · www.int-res.com 282 Mar Ecol Prog Ser 425: 281–296, 2011

first two are known as macronutrients while iron is decade before it is subducted, or mixed, below the bot- classified as a micronutrient (also known as a trace tom of the seasonal thermocline. While in the photic nutrient). Martin et al. (1990a) first brought attention to zone and above the thermocline, the nutrients in the the concept of providing a limiting trace nutrient to water contributes first to new primary production, and certain regions of the ocean to increase productivity. A then some of the organic matter is decomposed (regen- number of culture bottle studies, mesoscale ocean erated) to support further primary production. Eventu- experiments and ocean circulation models have clari- ally the water is subducted below the surface layer and fied the role that nutrient addition might have on starts its long journey through the deep ocean. When ocean productivity. this water again enters the photic zone after its cycle Increased productivity in the form of new primary through the deep ocean, its nutrients have been production will enhance the flow of energy through replenished by the rain of organic matter from the sur- the marine food chain. Most of the anthropogenic face ocean. activity in the ocean consists of hunting and gathering, Clearly, nutrients limit the capacity of the marine together with the transport of goods and people. Fortu- food chain to produce protein. The limited supply of nately, the low level of this usage means there is little nutrients that enters the surface ocean restricts the foregone opportunity (opportunity cost) in making new primary production, on which the regenerated increased use of the ocean for extra food production, in production and secondary production depend. Tyrrell contrast to attempting more intense farming on land. (1999) and many others discuss which nutrient in the There are many who see an aesthetic value in undis- surface ocean is limiting new primary production. turbed vast barren expanses of ocean. This view must Locally, new primary production may be limited by be weighed against the need of malnourished humans one or more elements that often include nitrogen, for economical protein. Humans have already ex- phosphorus or iron. As the surface water is advected ceeded the sustainable fish catch for the large mem- by the large ocean gyres, new inputs of iron or reactive bers of the marine ecosystem, which is a significant nitrogen from the atmosphere can relieve the limita- disturbance to the ocean ecology. We have now started tion. Rivers are also supplying new reactive nitrogen fishing down the food chain (Pauly et al. 2000). Is there as a result of the fertilisation of agricultural lands. a way to have both an adequate amount of protein for Nutrients that are carried below the photic zone before the poor and also a sustainable ocean ecology? they can participate in the generation of primary pro- Recent reviews consider the strategy of large-scale duction and the flow of energy to higher trophic levels iron fertilisation of the oceans for increasing productiv- are in a sense wasted. Each natural assemblage of ity (de Baar et al. 2005, Boyd 2008), but no review has phytoplankton that performs the new primary produc- contrasted ocean fertilisation using the micronutrient tion has different nutrient needs. Only certain organ- iron with other strategies to provide macronutrients. isms, called diazotrophs, can break the diatomic nitro-

While the present review focuses on such a contrast, it gen bond and directly use nitrogen gas, N2, which is does not treat the broader issues of the manipulation of available in vast quantities in the atmosphere. Dia- oceans as this has recently been discussed by Jones & zotrophs are thus able to increase the supply of nitro- Young (2009) and Johnston et al (1999). Costs of ocean gen for regenerated production. As diazotrophs need fertilisation are an important consideration but are not phosphorus, this suggests that on time scales of cen- compared here. Readers are instead referred to Boyd turies, phosphorus might be the ultimate limiting nutri- (2008) and Shoji & Jones (2001). ent in the sea. Phytoplankton photosynthetically converts dissolved inorganic material to organic particulate matter, which OCEAN CARBON CYCLE is strongly influenced by gravity. Senescent organic matter sinks below the surface ocean and is said to be At the heart of the dynamics of the ocean is the flow exported. The energy needed for photosynthesis in the of energy and materials. The vertical circulation of the ocean comes from the sun. Solar energy is transformed, waters in the ocean basins transports nutrients in a with the aid of chlorophyll, into chemical energy. While continuous cycle. The strong density gradient of the the level of sunlight regulates the rate of primary pro- seasonal thermocline inhibits vertical exchange duction on the time scale of a day, it is the availability of between the ocean surface mixed layer and the ocean nutrients over most of the ocean that limit the growth of abyss. The solar energy input to the photic zone sup- phytoplankton on time scales of months. ports the conversion of inorganic nutrients to organic Some of the senescent phytoplankton that has grown matter in a process known as primary production. in the surface ocean sinks below the base of the surface Assuming upwelling of 13 m yr–1 (Broecker & Peng mixed layer before it can be remineralised back to their 1982), surface water remains at the ocean surface for a inorganic components. The fraction of detritus that is Jones: Nourishment of the ocean 283

broken down in the seasonal thermocline is available to mary production on a yearly time scale (Gordon et al. the photic zone after winter deepening of the surface 1997). Thus these values for new primary production mixed layer. While the term ‘export’ is generally used also provide estimates of values for export of carbon rather loosely, I will use the term ‘deep export’ to mean from the surface ocean. the transport of material deeper than the top of the per- The global ocean models studied by Najjar et al. manent thermocline. The winter mixed layer depth, (2007) indicated a mean export of particles and dis- with the exception of portions of the polar ocean, is less solved organic matter (DOM) of 17 ± 6 Gt C yr–1. than 200 m (de Boyer Montegut et al. 2004). Most of the Assuming the exported matter is in the Redfield ratio exported matter is remineralised as it falls through the (by weight), C:N of (106 × 12):(16 × 14), this export pro- deep ocean and is not available to the photic zone for cess consumes 17 ÷ 5.7 = 3 Gt (3 × 1012 kg) N yr–1. This many decades. The exported biomass is approximately is more cycling nitrogen than the 1.55 Gt N yr–1 pro- in the Redfield ratio of C:N:P of 106:16:1, a robust aver- posed by Gruber (2008). If we assume the majority of age relationship for biological production on a long- this nitrogen is upwelled, and since Gruber (2008) pro- term, large-scale basis. As these elements are advected poses a representative nitrogen concentration in the by the deep ocean currents, they, with the major excep- deep ocean is 31 µM (M = mol l–1) or 434 × 10–6 kg N tion of the micronutrient iron, stay in a constant ratio. m–3, this implies a water upwelling volume of (3 × 1012) Once they enter the photic zone again, they bring with ÷ (434 × 10–6) = 6.9 × 1015 m3 yr–1. This suggests that the them the carbon that was exported years earlier. When organic carbon cycle is driven by a vertical flow of the concentration of dissolved carbon exceeds that 220 Sverdrup (Sv; 106 m3 s–1), a substantially higher needed to be in equilibrium with the atmosphere, the upwelling rate than that used by Sarmiento & Gruber excess carbon moves to the atmosphere as carbon diox- (2006) in their 2 box model. They suggested export ide. The nutrients are reused in new primary produc- fluxes closer to 10 Gt C yr–1 as more appropriate, tion and the process of cycling carbon through the deep implying an upwelling flow of 129 Sv. ocean continues. Therefore to the first order, steady- Of the 3 nutrients considered, iron is the most com- state photosynthesis, which drives the organic carbon plex in its interaction with the marine system. A certain cycle, does not lead to changes in the quantity of carbon concentration of iron is required for phytoplankton stored in the ocean. growth, and a higher concentration is required by dia- Bienfang & Ziemann (1992) estimated that new pri- zotrophs. A major source of iron in the surface ocean is mary production is approximately 7.4 Gt C yr–1. More deposition of dust from the atmosphere. The global recent estimates by Laws et al. (2000) provide a value distribution of atmospheric dust is markedly non-uni- of 12 ± 0.9 Gt C yr–1. Export production equals new pri- form, as illustrated in Fig. 1.

Fig. 1. Annual atmospheric deposition of iron (g Fe m–2 yr–1) after Mahowald et al. (2009) 284 Mar Ecol Prog Ser 425: 281–296, 2011

Some parts of the surface ocean have high concen- since it is mostly found in the surface ocean at concentrations of macronutrients but low chlorophyll concentrations above the Redfield ratio (Tyrrell 1999). Usually trations (referred to as HNLC regions). This lack of it is assumed that nitrogen-fixing phytoplankton con- chlorophyll productivity is believed to be substantially sumes phosphorus to keep the concentration of nitro- caused by a shortage of the micronutrient iron. Iron is gen and phosphorus close to the Redfield ratio for N:P not cycled in the same manner as other nutrients as it is in the long term. very insoluble in the surface waters (with high concen- Carbon dioxide is taken up by photosynthesis when trations of dissolved oxygen) and scavenged by falling light is available, while during dark periods it is particles. Iron attaches to falling detritus and is carried respired. Net consumption of carbon dioxide, i.e. the to the deep ocean. Phytoplankton needs iron because difference between photosynthesis and respiration, is chlorophyll cannot be synthesised, or nitrate reduced, of focus for the present review. without a C:Fe ratio of 100 000:1 (Martin 1990, Martin Photosynthesis produces a number of by-products et al. 1991). More recently, Klausmeier et al. (2008) that can affect global temperatures. The photosyn- placed the average composition of 15 phytoplankton thetic process leads to the production of compounds species at a C:Fe ratio of 16 500:1. Martin (1990) points that play a part in the formation of new atmospheric out that at his ratio, the ocean does not contain enough particles and hence cloud condensation. One such iron to support the conversion of all the nitrogen pre- compound is methyl iodide (CH3I). This compound, sent. In those areas where all the nitrogen has been when released from the sea surface, might lead to exported, enough iron must have been supplied during global cooling, via provision of cloud condensation the lifetime of the water on the surface to allow all the nuclei, as discussed by Smythe-Wright et al. (2006). nitrate to be consumed. Another compound produced during photosynthesis is The processes controlling the loss of iron in deep dimethyl sulphide (DMS), a gas of chemical composi- water are not clear. Johnson et al. (1997) pointed out tion (CH3)2S. Oxidation of DMS in the atmosphere is that the iron concentration at depth is not correlated involved in the formation of atmospheric sulphate par- with nitrogen concentrations, as one would expect ticles, which can exert a climate cooling effect directly from remineralisation of iron coming from the organic (by scattering and absorbing solar radiation) and indi- matter falling from the surface ocean. Rather, it seems rectly by affecting cloudiness and hence global albedo rapid scavenging decreases the iron concentration to a (Turner et al. 1996). low level which is maintained by iron binding ligands. Typically the upper ocean concentration of iron is low and rises to a value of about 0.6 nM in all deep oceans. FERTILISATION Scavenging appears to remove iron above a certain concentration. The concentration at a depth that might Martin et al. (1990a) suggested iron fertilisation as a be upwelled is not much above the half saturation con- way to encourage new primary production in HNLC centration of 0.12 nM found in culture bottle experi- regions. At much the same time, Martin et al. (1990b) ments by Fitzwater et al. (1996). pointed out the possible climate implications of in- In the case of nitrogen, the surface deposition is creasing local primary production. Subsequently there small, 54 Mt N yr–1 according to Duce et al. (2008) com- have been numerous in situ experiments in the South- pared with export of 1900 Gt N yr–1. The implication is ern Ocean (e.g. Boyd et al. 2000), the equatorial Pacific that, while nitrogen mostly travels with the carbon in (Martin et al. 1994, Coale et al.1996, 1998, Fitzwater et continuous cycle, much of the iron is lost from the deep al. 1996, Gordon et al. 1998) and the high latitude ocean and is not recycled. The notable differences in Pacific (Tsuda 2003, Takeda & Tsuda 2005). They all the recycling of the nutrients iron and nitrogen confirmed that enrichment of the surface HNLC water through the deep ocean are important in comparing increased the conversion of inorganic carbon to intentional fertilisation of the surface waters. organic matter locally. Nitrogen suffers a second order effect as it cycles For those regions deficient in macronutrients rather through the deep ocean. The organic nitrogen is ‘denitri- than iron, the addition of the limiting macronutrients fied’ to the gases N2 or N2O, which cannot be used by has been suggested as a way to increase productivity regular phytoplankton. Duce et al. (2008) placed the loss (Jones 1996). Those regions of near-zero surface nitro- –1 to N2O at about 5 Mt N yr . The organic nitrogen lost by gen are shown in Fig. 2. Three sources of increased this process is mostly replaced by the action of cyanobac- macronutrient supply have been suggested: (1) reac- teria. In addition, some organic nitrogen is supplied to tive nitrogen fixed by cyanobacteria; (2) upwelled the ocean from the atmosphere and by river inflows. nutrients from the thermocline; and (3) ammonia- Phosphorus, the other macronutrient considered, based products produced by the Haber-Bosch process seems to be remineralised more rapidly than nitrogen that converts atmospheric N2 to reactive nitrogen. Jones: Nourishment of the ocean 285

Fig. 2. Global map of nitrogen concentration in the surface ocean adapted from Levitus et al. (1994)

Yamasaki (2003) reviews sequestration options, which After remineralisation in HNLC surface water, iron is he sees as necessary in the short term. again limited. Hence, regenerated production does not generally occur locally. The deep exported carbon from the new primary production and its grazers are the MICRONUTRIENT ENRICHMENT only carbon stored in the deep ocean. The carbon remineralised in the seasonal thermocline is back in the HNLC regions occur where there are low rates of surface ocean by the next winter and is not considered atmospheric deposition of iron. The iron that is present stored. in the photic zone is either upwelled, as discussed by Gordon et al. (1997) for the HNLC waters of the equatorial Pacific, or is supplied by atmospheric deposition. MACRONUTRIENT ENRICHMENT The many experiments in HNLC waters have been summarised by Boyd et al. (2007), while Gulf of Mexico Reactive nitrogen fixed by cyanobacteria experiments are described by Markels & Barber (2001). In these experiments, soluble iron is added to Land-based agriculture has long practiced in situ the surface mixed layer. The phytoplankton nutrient nourishment of the soil by growing plants, such as limitation is relieved and photosynthesis is increased. legumes, that fix nitrogen. An obvious analogy for the The concentration of added iron decreases at a faster ocean is to arrange for the macronutrient nitrogen to rate than it is incorporated into organic matter (Fig. 3). be fixed by cyanobacteria. This was suggested by The soluble iron within the enriched patch is scav- Markels & Barber (2001), although they did not specu- enged by falling particles and transported out of the late on how this could be done. When there is ade- photic zone within about 10 d. The increase of phyto- quate nitrogen, other phytoplankton prospers at the plankton (Fig. 3b) is limited by zooplankton grazing as expense of cyanobacteria. In contrast, when inorganic nitrate remains within the enriched patch. When the nitrogen is in short supply, nitrogen fixers can be phytoplankton that remains from taking part in the expected to have an ecological advantage. However, new primary production dies, the chlorophyll concen- despite large expanses of oligotrophic ocean and ade- tration decreases as some dead phytoplankton is re- quate phosphorus supplies, there are limited amounts mineralised in the surface layer and some is exported of nitrogen-fixing cyanobacteria in the ocean. The pre- from the surface layer. According to Boyd et al. (2004), dominant cyanobacteria genera are Trichodesmium dilution is a minor cause for decrease in concentration and Richelia, although the importance of smaller uni- of particulate carbon in the enriched patch. cellular organisms is now being recognised (Zehr et al. 286 Mar Ecol Prog Ser 425: 281–296, 2011

) showed neither iron nor phosphate were –1 1.4 a 1.2 limiting their growth. 1.0 When cyanobacteria decay, the nitro- 0.8 gen originally fixed from the atmosphere 0.6 by the cyanobacteria enters the pool of 0.4 regenerated nutrients in the local surface 0.2 ocean. Devassy et al. (1978) showed ele- 0.0 vated concentrations of ammonia after a Iron conc. (nmol Fe l Iron 0 2 4 6 8 10 12 14 16 18 20 22 24 26 Trichodesmium bloom in the sea; a broad ) 6 range of nutrients were also released as –3 b 5 Trichodesmium decayed in culture bottles. Mulholland (2007) noted that 4 cyanobacteria might not export carbon 3 and nitrogen directly, as they tend to produce DOM which is taken up by bacteria. 2 Some of the cyanobacteria are grazed by 1 higher trophic levels and may then be ex- 0 ported as fecal pellets. However, since Chlorophyll conc. (mg m Chlorophyll 0 2 4 6 8 10 12 14 16 18 20 22 24 26 nitrogen levels are not rising, all of the Day fixed nitrogen is eventually exported either directly or through regenerated Fig. 3. Iron fertilisation results reproduced from Boyd et al. (2004). (a) Iron concentration. f: within the fertilized patch; j: outside the patch. Iron production or as a result of secondary was injected twice, on Day 0 and Day 6. (b) Phytoplankton growth, as mea- production. sured by chlorophyll concentration within the enriched patch Cyanobacteria need the macronutrient phosphorus. Sañudo-Wilhelmy et al. (2001) produce some evidence that 2001). Breitbarth et al. (2006) noted that Tricho- phosphorus limits nitrogen fixation in some regions of desmium does not fix N2 below 20°C, as it is only found the ocean. Mahaffey et al. (2005) support this view. in the tropical and subtropical ocean (Capone et al. When Cullen et al. (2002) talk of continuous fertilisa- 1997). Small nitrogen-fixing bacteria extend this range tion with iron and phosphorus, are they thinking of somewhat. Falkowski (1997) cites Letelier & Karl encouraging cyanobacteria to fix more nitrogen? In (1996) and others when stating that nitrogen fixation is the FeeP mesoscale experiments to examine these limited by iron availability. There is evidence that issues, Rees et al. (2007) found that in the north-east cyanobacteria are more common in areas of the ocean Atlantic, the ‘microbial community was likely to be with high dust input (and hence presumably with high limited or co-limited by one or more nutrients in addi- iron concentrations). tion to Fe and P […] and nitrogen fixation […] As a result of field studies in the central Atlantic, increased by up to 6 times and 4.5 times […]’ with Sañudo-Wilhelmy et al. (2001) reported that the nitro- addition of Fe and of Fe and P, respectively. gen fixation rates appeared to be independent of the There appear to be areas of local iron shortage dissolved iron concentration in the surface ocean. where iron scavenging exceeds upwelling and atmos- Their calculations suggest that the concentration of pheric deposition. These areas could be targets for iron iron required by cyanobacteria may be 2.5 to 5.2 times fertilisation for cyanobacteria conversion. There are higher than by ammonium-assimilating phytoplank- boundless mineral deposits of iron that can simply dis- ton. This would suggest that in iron-restricted situa- solve in sea water by reacting with acid. Markels tions with ample reactive nitrogen supplies, diatoms, (2002) suggested that bound iron, which may survive rather than cyanobacteria, use the available iron scavenging due to organic complexation, might be (Schmidt & Hutchins 1999). more effective for iron fertilization. Providing soluble Iron and phosphorus are not the only limiting nutri- iron and phosphorus to the photic zone in low-nitro- ents. Paerl et al. (1987) found that concentrations of gen, iron-limited regions could be expected to allow oxygen and DOM played a role in marine nitrogen an increase in production of organic nitrogen via fixation. The need for DOM was a clear result in their enhanced cyanobacteria activity. The role of DOM in culture bottle experiments. Fu et al. (2005) concluded the fixation of nitrogen by bacteria as well as the iron that dissolved organic phosphorus may be important biochemistry of the sea is unclear. The in situ fixing of in supporting cyanobacterial growth. Nitrogen-fixing nitrogen in the sea requires more mesoscale experi- bacteria when cultured by Needoba et al. (2007) ments to clarify the role of the various limitations. Jones: Nourishment of the ocean 287

Upwelled nutrients from the thermocline many other forms of inorganic nitrogen. Painter et al. (2008) deduced that urea provided 23 to 31% of the The waters near the top of the thermocline, but consumed nitrogen in any particular aquatic environ- below the photic zone, are another source of macro- ment. In some locations, phosphorus can be a co-lim- nutrients. Artificial upwelling of this thermocline water iting nutrient (e.g. Thomas 1969, DiTullio et al. 1993). has been considered as a means of fertilising the photic When nitrogen is the limiting nutrient, adding urea to zone. the surface ocean will encourage phytoplankton One difficulty for those interested in carbon storage growth and the conversion of inorganic carbon to is that, while the thermocline is rich in nutrients re- organic biomass. While reports of iron and phospho- mineralised in the deep ocean from organic matter, rus fertilisation in mesoscale experiments exist, no this organic matter also contained carbon. Such up- such studies on nitrogen introduction have been pub- welled water, because of its age, may have left the sur- lished, but an experimental pilot plant design has face ocean when the partial pressure of atmospheric been prepared by Jones & Otaegui (1997). However, carbon dioxide was lower. This component of the there are numerous culture bottle studies of nitrogen upwelled carbon may be undersaturated with carbon fertilisation of natural assemblages from oligotrophic dioxide at present atmospheric conditions. waters (e.g. Menzel & Ryther 1961, Tranter & Newell A Japanese research group (Toyota et al. 1991) 1968, Thomas 1969). raised up water in 1989 and 1990 from about 200 m These culture bottle experiments all show that in low depth. However, this did not produce a measurable nitrogen regions, adequate micronutrients are present increase in new primary production. The deep water to support additional primary production. Fig. 4 shows probably diluted too quickly to cause a change in a typical result, in which water from the Sulu Sea primary production measurable by the techniques (10° N, 122° E) was dosed with 8 µM of nitrogen in the used. form of urea as well as sodium phosphorus in the Red- I estimated above (see ‘Ocean carbon cycle’) that it field ratio. In this example it appears that most of the takes 220 Sv of upwelling to induce 17 Gt C yr–1 of new added nitrogen was consumed by Day 5, and senes- primary production in the photic zone of the world’s cence set in. ocean. The nutrients in 106 m3 (a Sverdrup second) of New primary production will continue until it has upwelled water will support the conversion of about exhausted all the added macronutrients (or if too

283 t of inorganic CO2 to organic carbon. To raise much was added, after new primary production has water takes energy. Lovelock & Rapley (2007) recently exhausted some other critical nutrient). Remineralisa- advocated using wave pumps to provide this energy. tion produces a set of regenerated nutrients able to The Japanese group used electricity. again undergo primary production. It is assumed that The artificial upwelling of the thermocline is not con- there will be an adequate flux of iron from the atmos- sidered further in this discussion of carbon storage, phere outside the HNLC ocean regions. This process because the high concentration of dissolved inorganic of production of biomass, decay and remineralisation carbon in the upwelled water means that enhanced constitutes a cycling of the nutrients. This cycling in carbon storage via enhanced photosynthesis will be the surface ocean of the added nutrient continues negligible. until the added nutrient is fully exported to the deep ocean. The exported fraction of new primary production is of interest in iron fertilisation of HNLC regions Haber-Bosch process (e.g. Trull et al. 2001). However, in the case of fertilisation by the limiting macronutrient, this new pri- Another way to provide the macronutrient nitrogen mary production export is not an issue, provided the is by using the Haber-Bosch process to break the dini- ocean region has an adequate supply of iron. In this trogen bond of atmospheric nitrogen. With a supply of case, eventually all of the added nutrient is exported energy, atmospheric nitrogen is combined with hydro- by a combination of new primary production followed gen supplied from steam or fossil fuels, and reacted by as many cycles of regenerative production as are over a catalyst to produce ammonia. The ammonia gas required. can be further reacted with carbon dioxide to produce urea. Agricultural activity uses much of this reactive nitrogen to enhance crop yields. Over-application of Phosphorus nitrogen fertiliser with its associated run-off has led to problems in rivers and estuaries. In low-nitrogen, low-chlorophyll regions of the Urea is readily taken up by phytoplankton (e.g. ocean, we need to consider the phosphorus concentra- Eppley et al. 1973, Sambrotto & Mace 2000), as are tion. In the northern hemisphere, phosphorus concen- 288 Mar Ecol Prog Ser 425: 281–296, 2011

20 one would choose to fertilise with our present level of Control knowledge. 8 µM (N) + (P) In addition to these 3 cases, the polar regions have 16 µM (N) + (P) adequate nitrogen and phosphorus levels, but the iron )

–1 15 concentrations are below those needed by both ammonia-consuming phytoplankton and diazotrophs. In regions where the phosphorus concentration is very low, it will be necessary to add phosphorus 10 obtained by mining phosphate rock if additional photosynthesis is desired. Thus nourishment can proceed by adding Haber-Bosch nitrogen with the phosphate (in situations with adequate iron) or by adding phos- 5 Chlorophyll conc (µg l Chlorophyll phate and iron to support diazotroph production of reactive nitrogen and regenerative production. The former option may be chosen if there is concern about the iron concentrations needed by diazotrophs. Lenton 0 01234567& Vaughan (2009) considered the capacity of either Days after fertilisation nitrogen or phosphorus to store carbon, but a much greater sequestration could be obtained by the combi- Fig. 4. Culture bottle results of fertilising water from the Sulu nation of nitrogen and phosphorus. If one also relaxes Sea. Control and enrichment with N + P are shown. A dosage the assumption that phosphorus is only supplied at the of 8 µM of nitrogen on Day 1 led to a maximum concentration of chlorophyll on Day 5, while the bottle with larger dosage rate of agricultural demand, the storage of carbon in had yet to peak on Day 7. Biomass was mostly diatoms. 2050 suggested by Lenton & Vaughan (2009) could be Modified from Harrison (2007) greatly exceeded. The process of phosphate and iron fertilisation in an example of natural ocean nourishment was observed tration, like that of nitrogen, is very low in surface by Subramaniam et al. (2008). The Amazon River ocean waters warmer than about 20°C (e.g. Sarmiento plume transports phosphorus and iron into the Atlantic & Gruber 2006). This suggests cyanobacteria such as Ocean, which supports the growth of diazotrophs Trichodesmium have consumed the phosphorus and which fix about 3 Mt N yr–1. provided reactive nitrogen to the upper ocean. How- In regions with negligible phosphorus concentration, ever in most of the rest of the low-nitrogen ocean, the addition of phosphorus obtained by mining may phosphorus concentrations are high enough to support support diazotrophs and subsequently regenerative additional photosynthesis if reactive nitrogen was sup- production. It is not clear how many of these regions plied by either the Haber-Bosch process or by would also need a higher concentration of iron. Adding cyanobacteria. iron to the phosphate is not difficult and would proba- Iron concentration plays a part in determining the bly be a prudent action. viability of fertilising with phosphorus for various regions of the ocean. Various situations of relevance follow: ADVECTION OF FERTILISED WATER (1) The iron concentration is too low for (ammonia- consuming) phytoplankton to multiply. Since we are The addition of iron to HNLC regions can effec- considering regions of low nitrogen, there must have tively steal other nutrients. Aumont & Bopp (2006) been adequate concentrations of iron in the past. Large found in their model studies that nutrient stealing regions with these characteristics are unlikely. reduced the global additional primary production by (2) The iron concentration is too low for diazotrophs 50% of what it would have been. In the unfertilised but sufficient for ammonia-consuming phytoplankton HNLC ocean, iron limits photosynthesis, and the to multiply; however, there is too little nitrogen. The excess macronutrients are exported by ‘Ekman flow’ addition of iron may enhance diazotroph production in to the subtropical gyres. When the macronutrients this case. are consumed (because of fertilisation) before the (3) There is adequate iron for diazotrophs but some surface waters arrive in these regions of adequate element other than phosphorus is missing. Paerl et al. iron input, the waters are now macronutrient-limited. (1987) reported a situation where neither iron nor As a consequence, iron nourishment of HNLC waters phosphorus addition (separately) enhanced nitrogen is unlikely to be a major contributor to managing cli- fixation. This is a difficult situation and not a region mate change. Jones: Nourishment of the ocean 289

Dutkiewicz et al. (2005) show in their model that if larger area than the patch initially fertilised, and this the dust supply to the world’s oceans were increased means that looking for exported carbon with sediment (effectively iron fertilisation), then large regions of the traps is not likely to capture even a representative temperate oceans would experience a decrease in pri- sample of the exported carbon. mary production because of macronutrient limitations. The extra primary production (resulting from the dust) in HNLC regions would export nutrients from the REMINERALISATION AFTER EXPORT surface ocean. These nutrients, following advection, might have otherwise been used in the temperate The depth at which the organic material is reminer- oceans. The global response of the model to additional alised depends on the species that prosper from en- dust is an increase of only a few percent in primary richment of the surface water. However, all 3 choices of production (and hence presumably also in export pro- providing nitrogen are likely to produce much the duction). same distribution. All 3 fertilisation approaches rely on Gnanadesikan et al. (2003) found much the same regenerated production to export most of the carbon. reduction of primary production when they modelled In contrast, HNLC regions with micronutrient fertilisa- patch fertilisation of the equatorial Pacific. As the iron- tion have to rely predominantly on new primary pro- fertilised patch drifted across the Pacific, it supported duction. Different forms of nitrogen may lead to differ- less primary production than a non-fertilised patch. ent species composition in the new primary production The surface ocean has a refreshment time of a decade, and different export depths. For example, diatoms with allowing ample time for atmospheric deposition of iron their silica framework are expected to be reminer- to eventually cause all the nitrogen to be exported alised at greater depths than small bacteria. We specu- from the unfertilised waters of the temperate oceans. late that the initial form of the nitrogen will have little Given that iron fertilisation leads to macronutrient impact on the export depth of regenerative production. stealing, it is interesting to consider whether there is a As well as exporting carbon from the surface ocean, similar effect for macronutrient fertilisation. The addi- some phytoplankton exports calcium carbonate. An tion of macronutrients will consume trace nutrients. example is coccolithophorids, which have an armour of

Might macronutrient enrichment of low nitrogen small CaCO3 plates. The loss of calcium carbonate regions of the surface ocean be another form of nutri- causes the CO2 partial pressure of the surface water to ent stealing? Could nourishment of one region cause rise, which is the opposite effect to what one might deficits in trace nutrients in some currently productive expect intuitively. The net effect of the export of coc- areas? At present, there are no areas of the ocean colithophorids is a smaller net reduction of partial pres- recognised as having limiting trace nutrients (except sure per unit of added nitrogen than for the export of iron). Bottle studies of enrichment with macronutrients diatoms. Particulate inorganic carbon (PIC) exported could determine if there are regions of the ocean that from the surface ocean has been estimated by Berelson lack enough trace elements to support further phyto- et al. (2007) to be in excess of 1.6 Gt C yr–1, but this plankton growth. quantity will decrease in the future because of ocean If only nitrogen were to be added in regions with acidification. Matear & Elliott (2004), in their modelling residual phosphorus, the export of the phosphorus in studies, thought that inorganic carbon production as a the organic matter could limit diazotrophs later in the result of enrichment might reduce the effectiveness of lifetime of the surface water. Gruber (2008) estimated sequestration of carbon by up to 25%. This fraction that diazotrophs fix 100/5.7 = 17.5 Mt N yr–1 and so probably depends on the concentration of silica, which using the Redfield ratio, consume 100/41 = 2.4 Mt P influences the number of diatoms present to compete yr–1. The excess P supplied to the surface ocean (dis- for nitrogen. If the species composition is much the cussed in ‘Strategies for ocean fertilisation’) is 155/7.2 same in the regenerated production (where most of the = 21.5 Mt P yr–1. Thus the least uncertain approach to export takes place) as in the new primary production, fertilisation would be to add the complete spectrum of the impact of PIC will be much the same for any nutrients. Artificial upwelling would accomplish such enrichment and will not be considered further. fertilisation, but is unfortunately not a promising The marine snow is remineralised in approximately enough method for providing nutrients to manage the Redfield ratio of elements, C:N:P, 106:16:1. Most of atmospheric carbon dioxide concentrations. the constituents of the organic matter (with the notable Advection of those nutrients remineralised in the exception of iron) return to the surface waters after surface waters means that regenerative production hundreds to thousands of years (see below). On return takes place in a different geographical location from of the deep exported matter (now in inorganic form in the new primary production. Thus, for macronutrient the Redfield ratio) to the photic zone, the sunlight- fertilisation, export to deep waters occurs over a much aided conversion to organic matter leads to no loss of 290 Mar Ecol Prog Ser 425: 281–296, 2011

stored carbon dioxide back to the atmosphere, pro- The time for water to return to the surface depends vided there is an adequate supply of atmospheric iron. on its depth and the location. The time for surface However, some of the exported nitrogen can suffer water to reach a location is termed the age (Matsumoto denitrification in the lower oxygen reaches of the deep 2007). Very loosely, the age of water at a depth of ocean and might not return to the photic zone in a suit- 1500 m is less than 300 yr in the Atlantic south of 40° able form for phytoplankton uptake. This reduces the latitude, less than 800 yr south of the equator and less reactive nitrogen in upwelled water and leads to a loss than 1200 yr elsewhere. Age, however, is not the time of the previously stored carbon. If the nitrogen is con- for the water to return to the surface. Modelling by Orr verted to N2O in the deep ocean, this powerful green- & Aumont (1999) showed that for remineralisation at a house gas reduces the climate benefits of the initial depth of 1500 m (in their case injection of a tracer) it storage of carbon. In the case of iron nourishment this took 200 yr for half the tracer material to reach the sur- was assessed by Jin & Gruber (2003) as quite substan- face at some locations and more than 500 yr at others. tial. The ventilation of the ocean refreshes the oxygen The ‘short’ residence time of exported carbon in the which is consumed in the remineralisation of marine Southern Ocean before the carbon returns to the surface snow, limiting the amount of N2O produced. A little of ocean partly explains the low efficiency for iron fertilisa- the marine snow settles on the ocean floor. Here the tion in the Southern Ocean. For example, Aumont & carbon is permanently sequestered, but the nitrogen is Bopp (2006) found that 75% of the carbon exported was remineralised and denitrified on the sea floor. This pro- upwelled and returned to the surface ocean in the first vides additional nitrogen to be upwelled, some of it 100 yr of iron fertilisation. On return of the exported mat- available to again sequester carbon. Ocean-wide nitri- ter, carbon escapes to the atmosphere, because the up- fication is on the order of 100 Mt N yr–1 according to welled nutrients lack iron. The cycle of macronutrients Gruber (2008), but there is considerable uncertainty. and iron is decoupled (Parekh et al. 2005). Other re- This is about a 5% loss of N each time decomposed searchers (e.g. Zeebe & Archer 2005) found greater car- marine snow is upwelled into the photic zone. This bon ‘leakage’. lowers the N:P ratio of upwelled waters and allows an opportunity for cyanobacteria to flourish. An important difference between relieving iron limi- SPECIES RESPONSE tation of macronutrient-rich waters and relieving macronutrient limitation is that iron is scavenged from Trophic level 1 the surface ocean and the thermocline by sinking particles. Parekh et al. (2004, 2005) were unable to resolve In the upper ocean, bacteria and phytoplankton whether the iron was lost, desorbed or complexed with compete for nutrients. Free bacteria utilise DOM organic ligands after it was scavenged. Dissolved iron released by phytoplankton. Larger organisms tend to concentration does not increase with the dissolved oxy- consume smaller organisms. The picozooplankton con- gen deficiency of the deep water as one would expect sumes smaller bacteria and are in turn consumed by from remineralisation of sinking organic matter. How- microplankton (2 to 10 µm). Azam et al. (1983) sug- ever, Bergquist & Boyle (2006) pointed out that, to make gested that this step provides a connection between a quantitative statement about the fate of the iron, one the bacterial cycle and the phytoplankton cycle. Bar- needs to know an equivalent effective scavenging rate. ren areas of the ocean are dominated by bacteria of The geographical location of the iron-limited water small size (<2 µm) with nutrients cycling between that is fertilised determines how quickly the exported phytoplankton, bacteria and zooplankton. Cullen et al. carbon is recycled to the surface ocean, and how much (2002) suggested that picoplanktonic organisms domi- of the introduced iron remains when the water again nate phytoplankton in oligotrophic waters, where their reaches the photic zone. small size gives them an advantage in obtaining the Macronutrient nourishment can be carried to regions limited nutrients available. The concentration of bacte- where iron is not the limiting nutrient. Here, the resi- ria is limited by grazing by picozooplankton (< 2 µm). dence time of exported carbon is different, as most of The small export ratio of the picoplankton biomass, the added nutrient is not lost but is instead available to discussed by Michaels & Silver (1988), results in nutri- be used again after upwelling. The scavenging of iron ents being reused many times before being exported (or at least the uncertainty about scavenged iron) to the deep ocean. Some of the nutrients in the micro- makes iron fertilisation of HNLC waters a less promis- zooplankton move up the size chain, while some is ing option for long-term storage of carbon than macro- converted to DOM to be used by bacteria. nutrient nourishment. Denitrification plays an equiva- Upon enrichment with iron in HNLC regions, the lent role to iron scavenging, by limiting carbon storage larger phytoplanktonic organisms are relieved of their time due to nitrogen addition to the ocean. iron limitation and can now access the available nitrate Jones: Nourishment of the ocean 291

and phosphorus. If there is adequate silica present, the The production of more harmful algal blooms (HAB) phytoplankton assemblage includes diatoms. Indeed, could be an undesirable outcome of enrichment if iron enrichment experiments report increases in the enhanced toxicity caused ecologically unwanted im- diatom populations. Diatoms store nutrients at a more pacts. A number of iron enrichment experiments pro- rapid rate than the picophytoplankton, and they can duced Pseudo-nitzschia spp. which have the capacity adjust their buoyancy to find nutrients (Sarmiento & to produce the potent neurotoxin domoic acid. Allsopp Gruber 2006, p. 279). Because of their size, diatoms are et al. (2007) pointed out that there was no evidence relatively efficient exporters of carbon. of harmful algae during the mesoscale experiments. The situation is different in the case of macronutrient However, Trick et al. (2010) created neurotoxin by enrichment. The species which responds most rapidly adding iron to culture bottles containing Pseudo- to macronutrient addition depends on the nutrients nitzschia spp. and found that the specific composition provided. When the nutrients encourage cyanobacte- of commercial iron substrates is a critical parameter in ria, the diazotrophs provide DOM, which is used by the degree of toxin production. Would the same result picoplankton with subsequent regenerated produc- be found in iron-rich areas where algae growth was tion. One assumes that on the second reuse of the triggered by the addition of macronutrients? The nutrients (regenerative production) it matters little answer to this question is not clear at this time. what form of nitrogen was supplied for additional new Zettler et al. (1996) found that iron benefitted only production. In the absence of silica, dinoflagellates are large diatoms in a series of bottle experiments in the expected to be more prominent. Harrison’s (2007) equatorial Pacific. Diatoms also favour ammonia over measurements found that Haber-Bosch urea supported nitrate (Eppley & Renger 1974). Cullen et al. (2002) diatom growth, suggesting that there was residual sil- suggest that red tide producing dinoflagellates prosper ica at the site investigated. in high-nutrient, low-turbulence situations. High con- The larger phytoplankton sinks faster upon senes- centrations of silica allow diatoms to outcompete cence, but the community composition is of secondary dinoflagellates. By restricting the concentration of importance in the case of macronutrient nourishment. nutrients provided during enrichment, one can avoid Those introduced macronutrients that are not exported high nutrient situations and possibly lower the risk of during new primary production are available for fur- HAB. ther photosynthesis in the future. As many have With more chlorophyll, increased production of DMS pointed out, the regenerated production leads to the is expected. The choice of fertilisation would impact on export equalling the new primary production (e.g. DMS production only through species differences. Eppley & Peterson 1979, Najjar et al. 2007, Yool et al. 2007). Carbon and nutrients are exported from the surface layer, either as particles or subducted as DOM. If Trophic level 2 all the new production (that is the first pass through the food web) was not exported, there would be a build-up Zooplankton provides another path for the export of of nutrients (e.g. nitrogen) in the upper ocean. This is carbon to the deep ocean. Its faecal pellets contribute to not observed, and there are no significant losses of the export of both carbon and nutrients from the surface macronutrients, for example through the sea surface. ocean. Zooplankton has a relatively slow growth rate However, the above considerations apply to spatial compared with phytoplankton. Thus, the concentration averages as pointed out by Plattner et al. (2005). The of phytoplankton in a patch of enriched water can ini- regenerated production may be many kilometres away tially increase without an immediately significant in- from the site of the original new production, as the cur- crease in grazing pressure. To estimate the new primary rents carry the surface waters containing the partially production caused by enrichment, the portion grazed by reformed matter many hundreds of kilometres. zooplankton and vegetarian fish must be included. The In the presence of adequate macronutrients, excess iron mesoscale experiments reported by Zeldis (2001) iron favoured the growth of larger phytoplankton in did not show much zooplankton increase inside the en- the culture bottle experiments of DiTullio et al. (1993). riched patch. The patch showed an 8-fold increase of pri- They did not observe greatly enhanced production but mary production 13 d after iron fertilisation, but less than a change in species distribution. Their results suggest 1% was consumed by zooplankton according to Zeldis that iron fertilisation of HNLC regions might lead to (2001). In a longer experiment (26 d), Tsuda et al. (2007) deeper export of carbon than enhancing the macro- found mesozooplankton mass was 3 to 5 times higher in nutrients in oligotrophic regions. A small percentage of the patch, and mesozooplankton grazing had a marked the exported organic matter reaches the sea floor, and impact on the phytoplankton concentration. again, iron fertilisation might deposit more carbon in In the CYCLOPS experiment, where phosphoric acid the deep water sediments. was added to the surface water, copepod egg abun- 292 Mar Ecol Prog Ser 425: 281–296, 2011

dance increased over the first few days (Thingstad et induced cyanobacteria production of nitrogen. They –1 –1 al. 2005). This response occurred as the concentration set a target of storing 2 Gt C yr (7.3 Gt CO2 yr ). This of chlorophyll decreased, and Thingstad et al. (2005) amount corresponds to the observed annual increase speculated that the extra phosphorus available in in atmospheric carbon, and to store all this using one heterotrophic bacteria is the signal for egg production. approach is very ambitious. They concludeed that this It is believed that the microbial community does not goal cannot be met by 1 injection of iron per year with contribute much to the supply of food for the higher characteristics of the SOIREE experiment described by trophic levels (Azam et al. 1983). Efficient grazing by Boyd et al. (2000). The iron injection in SOIREE zooplankton is required if energy captured by primary exported about 2000 t of carbon and, assuming the production is to flow to higher trophic levels. Rapid Redfield ratio, about 300 t of nitrogen were exported. egg production is needed. In order to achieve a pulse Such a small export of nitrogen had no impact on the of phytoplankton that lasts long enough for transfer to nitrate concentrations in a 1000 km2 patch of fertilised the next trophic level, the distribution of nutrients must water. If Boyd et al. (2000) had considered a number of be sufficiently concentrated. Nutrient infusion tech- iron injections during the summer instead of just niques able to produce the required level of nutrient 4 injections over 8 d, the quantity of carbon exported after a number of days of diffusion are discussed by would have been higher, and the limitation on primary Markels (2002) and Judd et al. (2009). production by predominantly diatoms might have been available silicon instead of available nitrogen. While Buesseler & Boyd (2003) and others discuss STRATEGIES FOR OCEAN FERTILISATION the export fraction of new primary production, this is an issue only in HNLC areas such as the Southern In situations where iron, phosphorus or nitrogen Ocean, where regenerated production is limited. As limit new primary production, a number of strategies pointed out above (‘Advection of fertilised water’), for ocean fertilisation are available depending on the however, the stealing of nutrients is an important issue location and the season. These are: for HNLC regions that casts doubt on the effectiveness (1) Iron fertilisation in HNLC waters. of iron fertilisation as either a sink of carbon or as a (2) Iron fertilisation in LNLC (low-nitrogen, low- method to increase the global new primary production. chlorophyll) waters with residual phosphorus. When does nourishment using Haber-Bosch nitro- (3) Iron and phosphorus fertilisation in LNLC waters. gen need to include phosphorus? Anderson & Sar- (4) Nitrogen fertilisation in LNLC waters with resid- miento (1994) found that the N:P ratio is always less ual phosphorus. than 16 in the deep ocean. They speculated that P is (5) Nitrogen and phosphorus fertilisation in LNLC remineralised more rapidly than N. Organic P is con- waters. verted to its inorganic form at a shallower depth than N The first 2 strategies can be considered micronutri- and so returns more quickly to the photic zone. Some ent fertilisation, while the latter 3 are macronutrient nitrogen also escapes the ocean as dinitrogen or nourishment. In those cases where there is sufficient nitrous oxide. This leads to a Redfield ratio of N:P of phosphorus but insufficient nitrogen (Strategies 2 and less than 16, and Falkowski (1997) suggested that the 4), it is assumed that the iron concentration is adequate dissolved inorganic phosphorus in the ocean needs on for phytoplankton to use any available nitrogen but average 2.7 µM of additional nitrogen to be in the Red- inadequate for cyanobacteria to use the phosphorus. field ratio. Some of this ‘missing’ nitrogen may be pro- The nutrients can be added over time either at a vided in the photic zone by nitrogen-fixing bacteria, particular geographic location or to the same patch but let us assume the nitrogen is all supplied by of water by following it as it is advected. The first macronutrient addition. A global upwelling estimate of approach (in which ocean currents bring unfertilised 129 Sv (4.1 × 1015 m3 yr–1) is equivalent to 13 m yr–1. water each day) can be considered similar to a number The nitrogen ‘deficit’ flux is 2.7 × 14 × 10–3 × 4.1 × 1015 g of independent mesoscale patch experiments of the N yr–1 = 155 × 106 t N yr–1 = 155 Mt N yr–1. As we would type that have been performed to date. The plume of expect, the deficit flux is considerably smaller (5%) new nutrients will with time become a plume of regen- than the estimate made earlier of the export flux being erated nutrients, becoming more dilute with time due 3 Gt N yr–1. Lenton & Vaughan (2009) suggest that the to diffusion and export. deficit is a higher percentage of nitrogen flux. In gen- Buesseler & Boyd (2003) addressed their question eral, the nitrogen in the organic carbon cycle is circu- ‘Will ocean fertilisation work?’ by considering observa- lating at between 1550 Mt N yr–1 according to Gruber tions made during mesoscale iron enrichment experi- (2008) and 3000 Mt N yr–1. Such fluxes of nitrogen are ments in the Southern Ocean and did not consider consistent with the earlier discussion of new primary fertilisation by macronutrient addition or by artificially production or export production. The flux of unused Jones: Nourishment of the ocean 293

phosphate (concentration 2.7 ÷ 16 µM) can be esti- period, new water rich in nutrients enters the surface mated to be 4.1 × 1015 × (2.7 ÷ 16) × 10–3 = 0.7 × 1012 mol ocean. There is some input of nutrients from the rivers yr–1. If nitrogen were added to combine with the sup- and the atmosphere as well as entrainment of nutrient- ply of unused phosphorus, then 106 × 0.7 × 1012 mol C rich water from the top of the permanent thermocline. –1 × –1 –1 yr = 74 44 Mt CO2 yr = 3256 Mt CO2 yr would In particular the concentration of iron and nitrogen will enter the organic carbon cycle. This result is approxi- change during the surface water’s decade-long life mately the same as that estimated by Marinov et al. time. (2008). After some length of time, with addition of new While the intentional macronutrient nourishment nitrogen only, all the excess phosphorus in the deep and micronutrient fertilisation with iron have many ocean in excess of the Redfield ratio would have been similarities, there are significant differences between fully utilised. Matear & Elliott (2004) suggest that cur- the 2 strategies, in terms of nutrient losses, regenera- rent surface phosphorus would support greater than tive primary production, nutrient stealing, techniques 0.8 Gt C of carbon export. for measuring storage and the cost of production of The discussion of the constraints of large-scale organic matter. In addition, the possible, unintended increases in ocean productivity does not mean that consequences could differ. such an increase will likely occur at once. Just as the Iron is rapidly scavenged from the ocean and replen- changes to the terrestrial ecology have been imple- ished only slowly by upwelling, diffusion or atmos- mented gradually (doubling grain productivity took pheric deposition. Creating new primary production half a century), Jones (2001) looked at the deployment by the addition of iron in nitrogen-rich water is not of 300 Haber-Bosch nitrogen manufacturing factories expected to lead to regenerative production in the (each of 0.6 Mt N yr–1 capacity) over 50 yr. Unless photic zone due to the loss of the added micronutrient phytoplankton with low phosphorus demand pros- in the surface waters. In situations with adequate sup- pered, such a scenario would more than use up the ply of iron, additional nitrogen could be supplied by residual phosphorus currently unused in the surface any of 3 methods. All these methods are expected to ocean. support both new primary production and regenera- The estimation of the amount of carbon stored by tive production until all the additional nitrogen is deep export as a result of fertilisation is worthy of dis- exported from the surface ocean or until another nutri- cussion. While the amount of new primary production ent becomes limiting. can be estimated from surveys of the enriched plume or Critics of ocean fertilisation have often focused on patch, the fraction that is finally exported is more diffi- the rapid return of the carbon exported by iron fertili- cult to measure directly. In the case of iron fertilisation, sation of the Southern Ocean HNLC region. Since it is the scavenging of the iron suggests that there will be assumed that most of the iron exported with the little regenerative production in the surface ocean. Ex- organic matter is lost in the deep ocean, some of the port will be limited to some fraction of the new primary carbon, nitrogen, etc. joins the HNLC region upon production. In the case of nourishment with nitrogen return to the surface, and the earlier addition of iron alone or nitrogen and phosphorus together, regenera- ceases to retain the previously exported carbon in the tive production will, over time, export all the new pri- ocean. mary production. However, the export will be spread Macronutrient stealing is a multipart processs. First, out over hundreds of kilometres as the surface water is nitrogen is exported from the surface ocean as a result advected around the ocean gyres. of supplying iron to one location. Next, the nitrogen depleted surface water drifts to a new location which has an adequate natural iron supply. This results in CONCLUSION diminished biological production at the new location. With macronutrient nourishment, additional micronu- Since Martin et al. (1990a,b) suggested using the trients are consumed and exported. Might they be regions of the surface ocean that contain unutilised needed for primary production as the water drifts to macronutrients to manage the climate, the concept has regions of atmospheric nitrogen deposition or dia- been further extended to embrace the purposeful zotroph activity? Where nitrogen or phosphorus limit introduction of the limiting nutrient to store carbon phytoplankton growth, culture bottle studies of natural while at the same time increasing the production of assemblages show that in most regions, the water con- marine protein. To understand the impact of ocean tains adequate micronutrients to respond to modest enrichment it needs to be recognised that the surface macronutrient nourishment. Clarification of the possi- water of the ocean, during its decade-long stay at the bility of significant micronutrient stealing awaits fur- surface, is transported large distances by the current ther study. However, the lack of reports of micronutri- systems that occupy each ocean basin. During this ent limitation, with the exception of iron, suggests that 294 Mar Ecol Prog Ser 425: 281–296, 2011

such a limitation may only become an issue for aggres- Boyd PW, Jickells T, Law CS, Blain S and others (2007) sive macronutrient nourishment. Mesoscale iron enrichment experiments 1993–2005: syn- Supplying the limiting macronutrient nitrogen seems thesis and future direction. Science 315:612–617 Breitbarth E, Oschlies A, LaRoche J (2007) Physiological the most promising approach at this time. Using this constraints on the global distribution of Trichodesmium — strategy, most of the export of carbon will not be in the effect of temperature on diazotrophy. Biogeosciences 4: new primary production cycle but will come from re- 53–61 generated production or from grazing by higher trophic Broecker WS, Peng TH (1982) Tracers in the sea. Lamont- Doherty Geological Observatory, Palisades, NY levels. On its return from the deep ocean, the added ni- Buesseler KO, Boyd PW (2003) Will ocean fertilization work? trogen again participates in photosynthesis in regions Science 300:67–68 where there is adequate iron, and it continues to store Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ the previously sequestered carbon. Further mesoscale (1997) Trichodesmium, a globally significant marine experiments are required to determine whether nitro- cyanobacterium. Science 276:1221–1229 Coale KH, Johnson KS, Fitzwater SE, Gordon RM and others gen nourishment can be carried out with the help of (1996) A massive phytoplankton bloom induced by an cyanobacteria or whether the certainty of the Haber- ecosystem-scale iron fertilization experiment in the equa- Bosch supplied nutrient (together with phosphorus in torial Pacific Ocean. 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Editorial responsibility: Hans Heinrich Janssen, Submitted: December 8, 2009; Accepted: October 18, 2010 Oldendorf/Luhe, Germany Proofs received from author(s): February 25, 2011