international journal global warming

Int. J. Global Warming, Vol. 6, No. 1, 2014 15

Copyright © 2014 Inderscience Enterprises Ltd.

Efficiency of carbon sequestration by added reactive nitrogen in ocean fertilisation

Martin W. Lawrence School of Geosciences, University of Sydney, Sydney, NSW 2006, Australia E-mail: [email protected] E-mail: [email protected]

Abstract: Addition of limiting nutrients to the surface waters of the deep ocean will lead to increased photosynthesis and associated biological productivity. Some of carbon taken up by phytoplankton will sink to the deep ocean, providing sequestration of carbon in the deep ocean. This paper considers nitrogen as the added nutrient and determines the losses in this sequestration process, taking into account a number of mechanisms. Other factors that impact on carbon sequestration are also taken into account, such as production of other greenhouse gases, and manufacture and distribution of nutrient. The overall efficiency of the sequestration process is found to be approximately 75%, depending on the form of the nutrient. That is, up to 75% of the carbon processed by photosynthesis (on adding nitrogen) can be sequestered. This is well in excess of sequestration estimates using iron as the added nutrient.

Keywords: ocean fertilisation; carbon sequestration; nitrogen; global warming.

Reference to this paper should be made as follows: Lawrence, M.W. (2014) ‘Efficiency of carbon sequestration by added reactive nitrogen in ocean fertilisation’, Int. J. Global Warming, Vol. 6, No. 1, pp.15–33.

Biographical notes: Martin W. Lawrence received his BSc (Hons) from the University of Sydney and his MSc and PhD from the University of New South Wales. He has worked for many years as a researcher and as a Scientific and Engineering Manager for the Australian Government and the United Nations. His work has focused on various aspects of ocean properties and processes. This paper was prepared while he was an Associate at the School of Geosciences, University of Sydney.

This paper is a revised and expanded version of a paper entitled ‘Efficiency of carbon removal per added reactive nitrogen in ocean fertilisation’ presented at Global Conference on Global Warming, Istanbul, July 2012.

1 Introduction

The addition of limiting nutrients to the surface waters of the deep ocean will lead to increased biological productivity, followed by sequestration of carbon in the deep ocean. This process is often referred to as ocean fertilisation. Due to the cycling time of the

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ocean currents, carbon that reaches the deep ocean will be sequestered (away from the atmosphere) for timescales on order hundreds to thousands of years (Yool et al., 2007).

A key question is: ‘What is the efficiency of this process in terms of sequestered carbon per atom of added nutrient?’ This issue has previously been examined with respect to adding the micronutrient iron, for example by de Baar et al. (2008) and Harrison (2013). Matear and Elliot (2004) have examined the efficiency following fertilisation with the macronutrient phosphorous. In the present work, we examine addition with the macronutrient nitrogen, which must be added in reactive form in order to be effective. Nitrogen is found to be the limiting nutrient for phytoplankton growth over 70% of the world’s ocean area.

The efficiency of this process is determined here for the case in which nitrogen is the limiting nutrient (that is, there is sufficient quantity of other nutrients, such as phosphorous and iron). Addition of reactive nitrogen will result in conversion of inorganic carbon to organic carbon, via photosynthesis, according to the Redfield ratio. Allowance must be made for ‘oceanic losses’, which are the various loss mechanisms on the path from organic carbon in the surface layer to carbon that is sequestered in the deep ocean, including the generation of any greenhouse gases. Further, allowance must also be made for ‘external losses’, which are losses that occur in processes that are external to the ocean, such as manufacture and transport of nutrient.

Additional nutrients result in new primary production, in which phytoplankton convert dissolved carbon dioxide into organic carbon. Some of this organic carbon will be exported to the deep ocean (i.e., sequestered), but much of it will be remineralised within the upper to mid ocean, below the permanent thermocline.

Upwelling will lead to these remineralised materials returning from below the permanent thermocline to the photic zone. Since these remineralised materials still contain the added nutrient elements, further cycles of photosynthesis will take place. From each cycle of upwelling and photosynthesis, some carbon will be exported to the deep ocean. After many cycles in the upper ocean, eventually the great majority of the carbon is exported to the deep ocean. On time scales of a year, export will have taken place of most of the organic carbon created by the new primary production. See Yool et al. (2007) for an analysis of the role of new nitrogen near the ocean surface in new primary production.

2 Method of analysis

It is not trivial to directly measure the efficiency of the sequestration process following addition of any nutrient. However, in the case of nitrogen, we can reasonably consider various loss mechanisms and find methods of evaluating their contribution to total losses. By combining all the loss mechanisms, an overall efficiency of this process may be calculated. The analysis presented here is based on global average values.

The oceanic losses are those that occur after addition of the nutrient to the ocean. These losses arise by a variety of mechanisms, each of which is described in turn below. Generically, they are: loss of reactive nitrogen from the ocean; production of greenhouse gas; efficiency of transfer of carbon between the atmosphere and the ocean; production of calcium carbonate; alkalinity effect on solubility of carbon dioxide; and fish effects.

Efficiency of carbon sequestration by added reactive nitrogen 17

The external losses are those that occur prior to addition of the nutrient to the ocean. The two non-trivial mechanisms for external losses are manufacture of nutrient and transport of nutrient. Each of these is addressed below.

3 Oceanic losses

This section addresses, in turn, the various oceanic losses (in sequestering carbon) that take place subsequent to addition of the reactive nitrogen to the ocean. A loss factor is determined for each mechanism of oceanic loss. These loss factors are determined as multiplicative factors that are combined at the end of this section.

3.1 Loss of reactive nitrogen from the ocean

3.1.1 Discussion

Sequestration of the generated organic carbon will be reduced by any loss of reactive nitrogen from the ocean.

As nitrogen is exported from the surface ocean to the mid-water depths, it is paired with carbon (in the Redfield ratio). Over time, much of this paired N and C will be split by bacterial action, remineralising the organic material. After a delay (typically years or decades), water from below the permanent thermocline containing this paired N and C will be upwelled to the surface ocean. The remineralised (inorganic) nitrogen is then available in the surface waters to be again combined with carbon through photosynthesis. Thus, to first order, all added reactive nitrogen would sequester carbon.

However, some reactive nitrogen is lost through a process of denitrification. The reduction in reactive nitrogen due to this effect is represented by the symbol DN.

The denitrification process occurs primarily in the low oxygen mid-depth region (below 100 m depth). The anaerobic reactions that remove reactive nitrogen (producing inert nitrogen, N2) take two forms: heterotrophic denitrification and anaerobic oxidation of ammonium.

3.1.2 Quantification

Our calculation of the fraction of reactive nitrogen that is lost to denitrification is based on the oceanic nitrogen budget developed by Gruber (2008). In total, Gruber (see Figure 1.14) finds that 1,120 MtN/yr of reactive nitrogen (both dissolved organic nitrogen and particulate organic nitrogen) is exported from the surface layer to below a depth of 100 m. Of this total, Gruber finds that 60 MtN/yr is converted to N2. These quantities are based on an assessment of previous work and strict attention to conservation of elements. Errors are estimated to be of order ± 30%. We use this global average ratio, producing the estimated loss of reactive nitrogen amounting to 5.4% due to denitrification. Hence, the value of the denitrification factor, DN, is (1–0.054) = 0.946.

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3.2 Production of greenhouse gas – denitrification

3.2.1 The N2O problem

The generation of any greenhouse gas must be factored into the calculation of net sequestration. The process of denitrification generates some nitrous oxide, N2O. A nitrous oxide factor, GN, is introduced to allow for this effect.

The addition of reactive nitrogen to the ocean will, in general, cause an increase in the quantity of nitrogen that is cycling through the ocean system. Such increased cycling can be expected to accelerate nitrification and denitrification processes, leading to the increased release of N2O (Fuhrman and Capone, 1991). This gas is a potent greenhouse gas, with a global warming potential 298 times that of CO2 (integrated over 100 years) (IPCC, 2007) and it also contributes to damaging the ozone layer. Fuhrman and Capone (1991) submit that there is a potential for ocean fertilisation processes to result in N2O release to the atmosphere, hence offsetting some of the gains from CO2 sequestration.

When remineralisation of organic matter occurs in a low oxygen environment, rather than just nitrate being formed (as is the case in a high oxygen environment), some nitrous oxide is formed. Low oxygen environments do not occur in the surface ocean (which is in communication with the atmosphere). Thus, the release of N2O to the atmosphere only occurs after a time delay (while the materials, sink, generate N2O, and finally are upwelled). Codispoti et al. (1992) reported that low oxygen waters (where O2 concentration is < 2 mL/L; < 43.3 μmol/kg) often contain high concentrations of N2O.

3.2.2 Quantification

As pointed out by Matear and Elliot (2004), increased N2O production may occur long after fertilisation. Law (2008) finds that measurement of N2O soon after ocean iron fertilisation show negligible N2O production, whereas long-term models suggest significant N2O production. This means that any calculation must consider the long-term large-scale situation, and cannot focus on immediate N2O production.

Our calculation of the denitrification factor is based on the oceanic nitrogen budget developed by Gruber (2008). Gruber finds that of the 1,120 MtN/yr of reactive nitrogen exported from the surface layer, some 4 MtN/yr is converted to N2O. All of this N2O subsequently escapes to the atmosphere. Following the Redfield ratio, 1 t of N combines with 5.68 t of C through photosynthesis. This quantity of C is equivalent to 20.8 t of CO2. Using Gruber (2008), 1 t of reactive nitrogen will produce 0.00561 t of N2O.

The IPCC (2007) (Working Group 1, Chapter 2.10) provides quantities of relevance to the global warming potential of nitrous oxide. The lifetime of N2O in the atmosphere is given as 114 years, while the global warming potential is given as 298 for a 100-yr time horizon. That is, for this time horizon, a unit mass of N2O has an effect on global warming that is 298 times larger than does a unit mass of CO2. Considering a 500-yr time horizon reduces the value of the global warming potential of N2O to 153. A longer time horizon would reduce it even further.

Taking into account the global warming potential, the N2O produced from 1 t of introduced N is equivalent to 298 × 0.00561 = 1.67 t of CO2. This is 8.03% of the CO2 sequestered. Thus, for a 100-year time horizon, due to denitrification we can expect that release of N2O will lead to an offset of CO2 sequestration corresponding to a nitrous oxide factor GN = 0.920.


3.3 Production of greenhouse gas – photosynthesis

A factor, Gp, is introduced to take into account the effect of any GHG generated before the initial export of nitrogen from the surface ocean.

Wingenter et al. (2004) produced a study of emissions of gases following fertilisation of the ocean by iron. As these gases are primarily produced by the process of photosynthesis, this study is also applicable to the gases following the fertilisation of the ocean by other nutrients including nitrogen. Law (2008) has examined measurements of greenhouse gas emissions following fertilisation with iron.

3.3.1 Dimethyl sulphide, (CH3)2S

Dimethyl sulphide (DMS) is a gas naturally produced as a result of photosynthesis in the ocean (Turner et al., 1996). Increased photosynthesis can be expected to increase the production of DMS. Oxidation of DMS in the atmosphere is involved in the formation of atmospheric sulphate particles, which can exert a climate cooling effect directly (by scattering and absorbing solar radiation) and indirectly by affecting cloudiness and hence global albedo (Turner et al., 1996).

Turner et al. (1996) suggest that, for iron fertilisation of the ocean, DMS cooling may have a larger climate effect than carbon sequestration. Further, Larsen (2005) concludes that the cloud formation over the (oligotrophic) tropical and subtropical regions (–30 S to +30 N) is substantially driven by DMS. This region has the greatest solar insolation and so reflectivity of sunlight is particularly important. Since nitrogen fertilisation is at its most effective in the oligotrophic ocean, this suggestion by Turner et al. (2006) of the importance of DMS cooling would be even more true for nitrogen than for iron fertilisation.

Law (2008) further addresses the issue of DMS production by ocean iron fertilisation. He reported that while most experiments had shown similar increases (1.5 to 1.6-fold) in DMS concentration, one experiment (in sub-arctic Pacific) actually showed a decrease in DMS concentration.

It can be expected that in most locations nitrogen fertilisation will have a positive effect on the global radiative balance due to the production of DMS. However, the present state of knowledge does not permit quantifying this effect. Hence, we will not include any factor of enhancement due to DMS production.

3.3.2 Other trace gases

Another compound that plays a part in the formation of new atmospheric particles and cloud condensation nuclei is methyl iodide. This compound, when released from the sea surface, might lead to global cooling as discussed by Smythe-Wright et al. (2006). Again, since this benefit is unquantifiable at present, its impact is ignored.

While the ammonia level in the upper ocean is expected to increase if compounds of ammonia are used to fertilise the ocean, any NH3 that escapes the sea surface will be washed back into the sea by rain. Thus, the escape of ammonia from the mixed layer is not of significance.

There may be small quantities of methane produced in photosynthesis. Measurements by Wingenter et al. (2004) showed a 1% change in the background level of methane in seawater following ocean iron fertilisation. Given the low concentration of methane in

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seawater, a change in methane concentration of 1% will be insignificant for the current calculations.

3.3.3 Summary of effect

The factor Gp (accounting for the effect of GHG generation prior to initial export of nitrogen from the surface ocean) is likely greater than unity. This corresponds to an amplification of the global cooling benefit from nitrogen fertilisation. However, given the difficulty in quantification, for our calculations we set Gp = 1.0.

3.4 Efficiency of transfer of carbon between atmosphere and ocean

Following a reduction in carbon dioxide concentration in the ocean, by Henry’s Law there will be a reduction in atmospheric CO2 concentrations. However, transfer of carbon dioxide from the atmosphere to the ocean can only occur at the ocean surface. Following CO2 depletion of the surface waters (subsequent to addition of nitrogen), these waters will absorb CO2 from the atmosphere only as long as these depleted waters remain in contact with the atmosphere.

The efficiency of the carbon dioxide transfer process will depend on the longevity in the surface ocean of the CO2 reduced waters. The efficiency also depends on the inherent time constant of the air-sea transfer process itself. The air-sea transfer efficiency will be designated by symbol ASTr.

Two time factors are needed to calculate the transfer efficiency, ASTr, across the air-sea interface following addition of nutrient. Each factor is characterised by an exponential time constant:

• residence time (τ) in the surface ocean (the time between when water is fertilised in the surface ocean and when it is subducted out of the surface layer)

• transfer time (T) for carbon dioxide to cross the air-sea interface.

The air-sea transfer efficiency is given by the equation:

TrAS 1/ exp(T / τ)= (1)

The value for the residence time, τ, is determined from the upwelling velocity (which is equivalent to the subduction velocity) and the depth of the surface ocean. The Lawrence Livermore National Laboratory ocean model described in Jones and Caldeira (2003) predicts an upwelling velocity of 12 m/yr. This value is consistent with the experimental result of Broecker and Peng (1982). The average mixed layer depth is interpreted from graphs in Figure 2 of Cropp et al. (2004) to be approximately 70 m. Using this value for the average surface ocean depth, DoS, the residence time τ = 70/12 = 5.83 yr = 51,100 h.

The value for the transfer time, T, is determined from the air-sea transfer velocity of CO2 and the depth (DoS) of the surface ocean. From Millero and Sohn (1992) (their Figure 6.26), using the global average wind speed of 7 m/s (Sweeney et al., 2007), the transfer velocity is 10 cm/h. Again, we will use the global ocean average surface depth, DoS, of 70 m. Then the transfer time, T, = 7,000/10 = 700 h.

Thus, the residence time is a factor of 72 longer than the transfer time. This directly leads to ASTr being near unity. Putting the numbers into equation (1), the air-sea transfer efficiency, ASTr = 1/exp(700/5100) = 0.986.


3.5 Alkalinity effect on solubility of carbon dioxide

3.5.1 Introduction to alkalinity and CO2 solubility

The solubility of carbon dioxide in seawater is dependent on temperature, pressure and the alkalinity level of the water. Addition of reactive nitrogen will change the ocean alkalinity and hence change the amount of CO2 that can be stored in the surface ocean. Thus, change in alkalinity will change the efficiency of carbon sequestration by addition of nitrogen.

Total alkalinity (AT) is defined as the seawater’s concentration of bases (negatively charged ions) that is capable of reacting with acid (positively charged ions). AT can be expressed as the sum of bi-carbonate, carbonate, hydroxide, and hydrogen ion concentration in seawater. Wolf-Gladrow et al. (2007) provide further information about total alkalinity.

A related parameter is the total inorganic carbon (CT), which is defined as the sum of all the inorganic carbon in the seawater. It is essentially a sum of the carbon in carbon dioxide, carbonic acid, bicarbonate anion, and carbonate anion. CT is an important parameter when making measurements related to the pH of natural aqueous systems. CT can be directly measured by acidifying a sample of the seawater.

Baes et al. (1985) provides empirically derived graphs of total alkalinity (AT) against total inorganic carbon (CT) at constant temperature. These graphs show that an increase in total alkalinity allows the oceans to store more carbon at constant partial pressure of carbon dioxide in the ocean (which closely tracks the partial pressure of carbon dioxide in the atmosphere). Baes et al. (1985) and Goldberg et al. (1980) provide more detail.

3.5.2 Photosynthesis and alkalinity

Photosynthesis affects the total alkalinity of the ocean since charged ions are consumed or generated in the photosynthetic chemical reaction, leading to a changed concentration of carbon dioxide in the surface ocean. This subsection provides quantification the effect on total alkalinity (of the surface ocean) of photosynthesis following addition of nitrogen-rich nutrient.

Photosynthetic reactions are set out below for five different nitrogen-based nutrients. The alkalinity created is shown in curly brackets around the appropriate term at the end of each of the following equations. In each equation, 106 moles of CO2 are consumed in the reaction. In determining the quantity of molecules in the reaction, the ratio of carbon and nitrogen compounds consumed is based on the Redfield ratio. Note that, although phosphoric acid is triprotic, at the concentrations it occurs in seawater, it is very largely in the form of the dihydrogen phosphate ion (as used in the following equations).

• Photosynthetic reaction for urea (creating one mole of alkalinity):

( ) ( ) ( ) ( ){ }

12 2 2 3 3 42 24 162 106

2 3

106CO 8 CO H PO 122H O NH H PONH CH O106O 7H 8HCO

−

+ −

+ + + ⇒

+ + + (2)

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• Photosynthetic reaction for nitrate (creating seventeen moles of alkalinity):

( ) ( ) ( ){ }

2 3 2 4 2 3 3 42 16106

2

106CO 16NO H PO 139H O NH H POCH O138O 17OH

− −

−

+ + + ⇒

+ + (3)

• Photosynthetic reaction for ammonium salts (creating 15 moles of acidity):

( ) ( ) ( ){ }

2 2 4 2 3 3 424 16106

2

106CO 16NH H PO 106H O NH H POCH O106O 15H

+ −

+

+ + + ⇒

+ + (4)

• Photosynthetic reaction for ammonium carbonate (creating one mole of alkalinity):

( ) ( ) ( ) ( ){ }

2 3 2 4 2 3 3 44 2 162 106

2 3

106CO 8 CO H PO 106H O NH H PONH CH O106O 7H 8HCO

−

+ −

+ + + ⇒

+ + + (5)

• Photosynthetic reaction for ammonium hydroxide (creating one mole of alkalinity):

( ) ( ) ( ){ }

2 4 2 4 2 3 3 42 16106

2

106CO 16NH OH H PO 91H O NH H POCH O106O OH

−

−

+ + + ⇒

+ + (6)

Equation (2) shows that for fertilisation with urea, a net 1 mole of total alkalinity, AT, is generated for every 106 moles of carbon dioxide being captured in phytoplankton. As a result, total alkalinity increases by 1% (1/106) of the moles of carbon converted to organic form. Equation (3), for fertilisation with nitrate (for example, sodium nitrate), shows 17 moles of total alkalinity are generated for every 106 moles of carbon dioxide being captured in phytoplankton. As a result, total alkalinity increases by 16% (17/106) of the moles of carbon converted. In contrast equation (4), for fertilisation with ammonium salts (excepting the two special cases shown in the following two equations), shows total alkalinity decreasing by 14% (15/106) of the moles of carbon converted. Just as for fertilisation with urea, fertilisation with ammonium carbonate or ammonium hydroxide creates one mole of total alkalinity. Table 1 For various nitrogen-based nutrients added to seawater, this table shows the fractional

change in total alkalinity, AT, (middle column) and the fractional change in total inorganic carbon, CT (right hand column)

Nutrient Change in AT (moles of

alkalinity/mole of carbon converted)

Change in CT (moles of CT/mole of carbon

converted) Urea AT increases by 1% 1.01 Nitrate AT increases by 16% 1.19 Ammonium salts AT decreases by 14% 0.83 Ammonium carbonate AT increases by 1% 1.01 Ammonium hydroxide AT increases by 1% 1.01

Note: The fractional changes are as a fraction of the quantity of carbon converted into organic form.

The effects on total alkalinity (normalised to one mole of carbon converted), for the various types of nutrient added, are set out in Table 1. Also shown in Table 1 is the resulting change in total inorganic carbon, CT, that can be supported by this new total


alkalinity, AT (assuming atmosphere-ocean equilibrium in CO2 partial pressure). An empirical relationship between AT and CT (both expressed as μmol/kg) is provided in Figure 5.3 of Baes et al. (1985), for constant partial pressure of carbon dioxide. This figure shows a linear relationship δCT = 1.20 × δAT, where δ refers to an incremental change in the parameter. In Table 1, this factor of 1.20 is used to convert from the change in AT to the corresponding change in CT.

The parameter Sphoto is defined as the fractional reduction (or increase) in the quantity of organic carbon that is produced due to the change in solubility that results from photosynthesis affecting alkalinity. Sphoto is simply the change in total inorganic carbon CT.

For example, from Table 1, for fertilisation with urea, Sphoto = 1.01, while for fertilisation with nitrate, Sphoto = 1.19. In these two cases, the increase in alkalinity results in an enhancement of the effect of fertilisation on the quantity of carbon that can be sequestered. With the understanding of these effects, the efficiency of carbon sequestration can be increased by an appropriate choice of nitrogen-based nutrient.

While ocean acidification is not the focus of this paper, it is evident from equations (2) to (6) that fertilisation with nitrate (in comparison with the other nutrients) will have a significantly larger effect on combating ocean acidification.

3.6 Production of calcium carbonate

Another mechanism that affects the efficiency of the carbon sequestration process is the production of calcium carbonate by phytoplankton, some of which make body parts from CaCO3. This mechanism can be explained by consideration of the generation of CO2 concomitant with production of CaCO3.

Riebesell et al. (2000) use laboratory experiments to examine the calcium carbonate production for two dominant marine calcifying phytoplankton species, the coccolithophores Emiliania Huxleyi and Gephyrocapsa oceanica. They show that carbon in solution is converted in the ratio of 0.9 into calcium carbonate to 1.0 into organic carbon. This ratio value is for present-day levels of atmospheric CO2 (the ratio varies with CO2 concentration).

The chemical process of formation of CaCO3 may be represented by the following equation.

23 2 2 3Ca 2HCO CO H O CaCO+ −+ ⇒ + + (7)

Thus, for every molecule of calcium carbonate produced, one of carbon dioxide is released.

Combining this with the ratio from Riebesell et al. (2000), we have that carbon taken up in producing coccolithophores goes 0.9 to organic carbon, 1.0 to calcium carbonate and 1.0 to carbon dioxide. Thus, there is a loss of 1/(0.9+1+1) = 34.5% in capture of carbon when photosynthesis leads to coccolithophores. We assume that this ratio will be appropriate for other species of coccolithophore and other calcifying phytoplankton such as foraminifera.

To assess the role of calcium carbonate production on sequestration efficiency for any area of the ocean, it is necessary to estimate the fraction of calcifiers in the phytoplankton assembly. A means of estimating this is to use the existing ratio of particulate inorganic carbon (PIC) (which is primarily calcium carbonate) to particulate organic carbon (POC).

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The molar export ratio, PIC-flux:POC-flux from the euphotic zone, was determined by Sarmiento et al. (2002) for the various areas of the world’s oceans. They used a technique based on alkalinity and nitrate data and found values of the ratio varied from 0.3% up to 9.9%. More direct measurement of PIC and POC data in limited locations show reasonable agreement with these values (Balch and Kilpatrick, 1996; Poulton et al., 2006). A simple average of the ratios provided by Sarmiento et al (2002) provides an average global export ratio of PIC:POC of 5.0%.

Combining the loss of 34.5% on producing calcifies with the 5% abundance of calcifiers provides a loss in efficiency of 1.7%. A factor Scarb is used to account for this effect, Scarb = 0.983.

3.7 Fish effects

Addition of reactive nitrogen captures carbon through the process of photosynthesis by plants. However, there can be a reverse effect from animals. Mechanisms that might be of significance are: firstly, respiration of fish and zooplankton; and secondly, capture and consumption of marine fish by humans. These two effects are considered here.

The first ‘fish’ factor that offsets the sequestration of carbon is the respiration of carbon by fish and other oxygen-breathing organisms. The respiration process inherently combines oxygen with the organic carbon. The CO2 generated by this process is returned to the surface ocean by the fish. However, there is no loss of reactive nitrogen in this process. As long as the fish (which now has this nitrogen in its body) does not leave the ocean, the chemicals will be returned to the oceanic system. The decaying fish, faecal pellets, and bones will all interact with the ocean environment. There is no loss of the reactive nitrogen. Thus, there is negligible reduction in uptake efficiency due to respiration.

The second ‘fish’ factor is the capture and consumption of marine fish that have incorporated some of the introduced nitrogen into their biomass. This can be considered to be a loss of new primary production. If the reactive nitrogen is removed from the ocean, it will no longer by available to sequester carbon in the ocean. However, within the fish the nitrogen is associated with carbon that has been captured in the ocean. Thus, it is necessary to consider what happens to this fish catch. The fate of the carbon in fish catch is complex. Some fraction of fish catch will meet each of the following fates:

1 thrown back into the ocean

2 buried on land

3 consumed by humans or other animals

4 burnt.

Much, but not all, of this will not be releasing CO2. To quantify this complex effect, we employ the following reasoning, following Jones

(2004). Pauly and Christensen (1995) suggest that exchanges between trophic levels are 10% efficient. Thus, trophic level 2, zooplankton, would have 10% of the carbon in phytoplankton and trophic level 3, fish, would have 1% of the carbon in phytoplankton. Carnivorous fish, at trophic level 3.5, would have an even lower percentage of the carbon in the phytoplankton. We assume that 1% of the carbon is incorporated in fish. Next, we assume that 50% of the extra fish (resulting from added nitrogen) are captured and taken


from the ocean. This is a high, and hence conservative, estimate. Using these assumptions, an allowance factor of 0.995 is made for the extra fish taken from the ocean as a result of adding nitrogen. That is: FE = 0.995.

3.8 Other oceanic losses

There are several other mechanisms for potential oceanic losses that have been considered, but are not explicitly analysed here. These include the following:

1 The addition of nitrogen might have some effect on the population of cyanobacteria. Due to the uneven distribution of cyanobacteria globally, as well as the possibility of adding phosphorous, this effect is complex and may be avoided.

2 Major oceanic circulation patterns are assumed to ensure that upwelling of remineralised mid-depth water take place in oligotrophic conditions.

3 It is assumed that the time period for which nitrogen added to the ocean is not matched to associated carbon is a negligible fraction of the sequestration time.

Further work could possibly confirm that these three issues are less significant than those for which an analysis is presented here.

3.9 Combination of oceanic losses

The total oceanic loss, Loce, in transforming organic carbon into sequestered carbon, is simply the product of all the above factor losses.

oce N N p Tr photo carb EL D G G AS S S F= × × × × × × (8)

Table 2 sets out the various factors that contribute to the total oceanic loss, together with the combined effect. Three nutrients are presented here; other nitrogen compounds were considered but they produced greater loss values. Table 2 Oceanic loss values for selected nutrients

Ammonium hydroxide and urea Nitrate

Loss of reactive nitrogen from the ocean, DN 0.946 0.946 Production of GHG by denitrification, GN 0.920 0.920 Production of GHG by photosynthesis, Gp 1.000 1.000 Air-sea carbon transfer efficiency, ASTr 0.986 0.986 Photosynthesis-alkalinity effect, Sphoto 1.010 1.190 Production of calcium carbonate, Scarb 0.983 0.983 Fish effects, FE 0.995 0.995 Total oceanic loss, Loce 0.848 0.999

Expressed as percentage, the total oceanic loss (in transforming organic carbon into sequestered carbon) is 15.2% for both ammonium hydroxide and urea, while for nitrate it is a remarkably low 0.1%. The only oceanic component factor that is dependent on the nutrient type is the photosynthesis-alkalinity factor. The very high efficiency in the case of nitrate is a direct result of the photosynthesis-alkalinity effect leading to an

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amplification of the carbon sequestration (which counteracts the losses resulting from the other mechanisms).

4 External losses

This section addresses, in turn, the losses in external processes that release greenhouse gases prior to addition of reactive nitrogen to the ocean. A loss factor is determined for each significant mechanism of external loss. The first significant mechanism is CO2 emission during the manufacture of the nutrient. The second significant mechanism is CO2 emission during transport of nutrient.

4.1 Manufacture of nutrient

The nutrient under consideration here is reactive nitrogen. There are several options for the production and delivery of reactive nitrogen. In each case, the first step is the production of ammonia (NH3) using natural gas, coal or other energy source. Hydrogen gas (H2), supplied from the steam reforming of natural gas feedstock, is reacted with atmospheric nitrogen gas according to the following equation:

2 2 3N 3H 2NH+ ⇒ (9)

Carbon dioxide will be released directly to the atmosphere as part of the chemical synthesis of ammonia, assuming fossil fuels are providing the energy requirements of this reaction.

The IPCC (2006) provides CO2 emission factors for the manufacture of ammonia. Using a modern plant with conventional reforming, the emission factor is 1.694 t of CO2 for each t of NH3 produced. This may be expressed as 0.561 t C emitted per t N produced as ammonia.

An alternative form of nitrogen is urea, a compound manufactured from the ammonia produced by the first step. The reaction combines ammonia and carbon dioxide to produce urea, in a two-step process which overall is as follows:

3 2 2 2 22NH CO NH CONH H O+ ⇒ + (10)

Note that in this reaction carbon is bound into urea. Thus, in modern urea plants, much of the CO2 from ammonia production is taken up again in the urea production. The IPCC (2006) provides an emission factor in the range 2 to 7 kg CO2 per t urea. Assuming the worst case (7 kg), this may be expressed as 0.008 t C emitted per t N produced. For the full process, including the initial ammonia production, there are thus 0.569 t C emitted per t N produces as urea.

A further alternative form of nitrogen is as nitrate ions. Nitric acid is produced from ammonia by an oxidation reaction that is achieved via several consecutive processes. Overall the reaction may be represented as:

3 2 3 2NH 2O HNO H O+ ⇒ + (11)

The greenhouse gas emissions during this conversion consist of N2O, which is generated as an unintended by-product (IPCC, 2006). The IPCC (2006) provides an emission factor of 2 kg N2O emitted per t of HNO3 produced, applicable to a modern plant fitted with


non-selective catalytic reduction (NSCR). To convert to CO2 equivalent, the relative global warming potentials N2O to CO2 must be applied. This ratio is 298 (IPCC, 2007), leading to a carbon equivalent (for N2O emitted) of 0.731 t C emitted per t N produced. For the full process, including initial ammonia production, there are thus 1.292 t C emitted per t N produced as nitrate.

To determine the efficiency loss due to the manufacturing process, it is necessary to compare the quantity of carbon emitted in producing the nutrients with the quantity of carbon taken up by phytoplankton following fertilisation. The average Redfield ratio informs that there are 6.63 carbon atoms for each nitrogen atom. Taking into account atomic weights, this means one tonne of reactive nitrogen corresponds to 5.68 t of carbon. Table 3 sets out the efficiency loss due to manufacture for three different nutrients. Table 3 Efficiency loss due to nutrient manufacture for three forms of reactive nitrogen

C (t) released per t of N manufactured

C (t) converted to organic form per t of N added Efficiency loss

Ammonium 0.561 5.68 9.88% Urea 0.569 5.68 10.02% Nitrate 1.292 5.68 22.75%

4.2 Transport of nutrient

The nutrient must be transported from the site of production to the site of distribution. There are a variety of possibilities for achieving this transport. For this analysis, we assume that transport is by a ship powered by fossil fuel.

Here, we consider a method for calculation of ship emissions. The calculation is begins with setting a target nitrogen concentration (which is based on not exceeding natural chlorophyll concentrations). The next step is to calculate how much ship steaming time is required to cover an ocean volume with this concentration. The final step is to determine the ship emissions that will occur in achieving this coverage. Global values are used for environmental parameters and typical values are used for ship characteristics.

4.2.1 Target chlorophyll concentration

The rate of distribution of nitrogen should be limited to that which will raise phytoplankton concentrations to the values seen in regions of ocean upwelling. This will restrict phytoplankton levels to the healthy levels seen in areas of upwelling and avoid the excessive levels seen in harmful algal blooms. Chlorophyll concentration is an easily measured proxy for phytoplankton concentration. So we need a target chlorophyll concentration that meets this upwelling criterion.

Figure 1 and Table 1 of Echevin et al. (2008) show values of chlorophyll concentration in the Peruvian upwelling of up to 5–10 mg Chl/m3 from both ship-collected data and SeaWIFs data. Table 2A of Pennington et al. (2006) shows a mean values for chlorophyll concentration at the sea surface in the subregion ‘Peruvian Coastal Upwelling’ of 2.55 mg Chl/m3 from ship-collected data and 2.27 mg Chl/m3 from SeaWIFS data. The subregion ‘Peruvian Coastal Upwelling’ is bounded by 4–15° S; 0–250 km offshore. Note that the highest chlorophyll concentrations occur in the region

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0–100 km from the shore. The chlorophyll concentration in this region will be higher than the above values. While this fact is stated by Pennington et al., and is evident from SeaWIFS colour-coded figures, a breakdown of concentration values is not provided.

In summary it would appear that, when most productive, the Peruvian upwelling generates chlorophyll concentrations in the range 5–10 mg Chl/m3. For the following calculations, the target chlorophyll value (from addition of nitrogen) is chosen to be 4 mg Chl/m3.

4.2.2 Target concentration of nitrogen

Riemann et al. (1989) provide values for the relationship between chlorophyll and organic carbon in phytoplankton. Results are provided for a number different phytoplankton species at various levels of nutrition. For the current purpose, the relevant values are those for well-nourished phytoplankton. The average percentage of chlorophyll-a in well-nourished phytoplankton is 3%. Using this percentage, we convert the target chlorophyll concentration to a target organic carbon concentration of 133 mg/m3.

Then, using the Redfield ratio and molecular weights, this is converted to a target nitrogen concentration of 1.68 mmol/m3.

4.2.3 Ship characteristics

In order to calculate the CO2 emissions, various ship parameters are needed. A typical ship capable of the required task would have a speed of 25 km/hr and consume fuel at a rate of 30 tonne/day. Using data from the US Energy Information Administration (USEIA, 2011) provides a value of 2.81 t CO2 per tonne of fuel consumed, corresponding to daily emissions of 84.3 t CO2 per day, which is 23.0 t C per day.

4.2.4 Volume fertilised

The volume fertilised, per day, is calculated by combining the distance steamed by the ship, with the swath width of the distribution of nutrient, and depth of the surface mixed layer.

Using the above ship characteristics, the distance steamed by the ship is 600 km/day. The swath width is the effective width of nutrient that is laid down by the ship as it

traverses the ocean. Subsequent to initial laying down the nutrient, it will spread by processes of diffusion and mixing. Boyd et al. (2007) report that the time to maximum chlorophyll concentration (after fertilisation) was 4 to 8 days, across a set of 12 fertilisation experiments based on iron. In this period, considerable movement and spreading of the fertilised patch takes place as is exemplified by the SOIREE iron fertilisation experiment (Abraham et al., 2000; Boyd et al., 2000). The SOIREE experiment used a track separation of 600 m to form a patch 7 km in diameter. Abraham et al. (2000) find a rate of stretching of the patch (from ship observations of the resulting phytoplankton bloom) of 0.07 per day. This corresponds to a change in diameter of the patch over 6 days of 1.076 = 50%. In the current analysis for CO2 ship emissions, we choose 600 m track separation, as used in SOIREE. This track separation sets an effective swath width for the nutrient.


The surface mixed layer mixes throughout its depth on a daily basis, due to a process of day-night heating and cooling of the ocean surface. Thus, nutrient will quickly mix through this layer. The global average mixed-layer depth is interpreted from graphs in Figure 2 of Cropp et al. (2004) to be approximately 70 m, averaging across all oceans of the world. A more appropriate value for macronutrient fertilisation ocean regions is 50 m (ignoring high latitude waters, which are inappropriate for such fertilisation). This value is used in later calculations.

Using the above parameters, the volume fertilised is 18 × 109 m3 per day.

4.2.5 Efficiency

Combining the target nitrogen concentration with the fertilised volume provides a distribution rate of 423 t N per day. This rate will, by the Redfield ratio, convert carbon to organic form at the rate of 2,400 t C per day. This must be compared with the transport (ship) emissions of 23 t C per day. The loss of efficiency by these transport emissions is thus 0.96%.

There will also be ship emissions during transit from port to the area to be fertilised. This effect, which of course depends on the transit distance, turns out to be a much smaller effect. Using typical values for transit distance and taking account of the densities of the three nutrients, it will increase the loss of efficiency due to transport: for urea to 0.98%; for ammonium to 0.99%; and for nitrate to 1.03%.

4.3 Combination of external losses

The overall loss due to external processes may be determined from the above. We have assumed that modern chemical plants are used. If an older plant were used, the calculation would need to be repeated using the emission factor for that plant type. Table 4 sets out the various components and the total external loss for three nutrients. Table 4 Losses due to external processes, for three forms of reactive nitrogen

Manufacture loss Transport loss Total external loss, Lext Ammonium hydroxide 9.88% 0.99% 10.9% Urea 10.02% 1.00% 11.0% Nitrate 22.75% 1.03% 23.8%

5 Total losses

The results of the above analyses, in combination, provide an overall efficiency for carbon sequestration following addition of the macronutrient nitrogen. The losses, Loce, in going from organic carbon to sequestered carbon are independent of the external losses, Lext, in manufacturing and transporting nutrients. Hence, the percentage losses must be added to obtain the total loss. These losses are set out in Table 5. Note again that the reference level for these losses is the case in which all added reactive nitrogen leads to sequestered carbon, following the Redfield ratio.

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Table 5 Total percentage losses in the process of sequestering carbon from initial organic carbon produced

Ocean loss, Loce External loss, Lext Total loss

Ammonium hydroxide 15.2% 10.9% 26.1% Urea 15.2% 11.0% 26.2% Nitrate 0.1% 23.8% 24.9%

6 Discussion

The losses in sequestration potential, subsequent to adding reactive nitrogen to the ocean, have been calculated for both oceanic losses and losses external to the ocean. A variety of loss mechanisms have been identified and quantified.

The sum of these losses in the sequestration process is shown in Table 5 to lie between 24.9% and 26.1% for the three nitrogen-based nutrients considered. These values are applicable for nutrient manufacture using modern techniques. Although not presented here use of some other forms of nitrogen-based nutrients, e.g., ammonium salts, resulted in significantly worse efficiencies.

It is evident from Table 5 that, while the three different nitrogen fertilisers have similar overall efficiency, the oceanic and external components of this loss is very different in the case of nitrate, which has very low oceanic losses, but much higher external losses.

The above calculations have been performed conservatively. That is, the underestimation of losses has been avoided by making suitable choices of parameters and techniques. For example, the size of nitrous oxide effect (GN) that was used is based on a 100-year time horizon. However, there are two effects that will reduce the effect of nitrous oxide. Firstly, for a longer time horizon, the offsetting effect of N2O will be diminished; for a 500-year time horizon, the nitrous oxide factor is reduced to GN = 0.959. Secondly, some of the nitrous oxide that is formed in the ocean will not be ventilated to the atmosphere for periods longer than 100 years.

The quantification of losses is based on global averages. The technique can be adjusted somewhat to consider regional effects, for example the fraction of carbon that is incorporated into calcium carbonate depends on the regional phytoplankton assemblage. In another example, regional rather than global values may be used to calculate the loss resulting from nutrient transport. Given the fixed target for chlorophyll level, some operational parameters (e.g., swath width and rate of infusion of nitrogen) will also depend on measurements made at the site (of parameters such as mixed layer depth, diffusion rate, and phytoplankton growth rate).

It is of interest to compare the efficiency of carbon sequestration for nitrogen fertilisation with that for iron fertilisation, a subject that has a wider literature. The inefficiencies in sequestration by iron fertilisation are described by de Baar et al (2008) and Harrison (2013). While iron fertilisation has the immediate benefit that only a small quantity of iron is required to create organic carbon, the process has inherently high inefficiency in sequestration of carbon. The fundamental reason for this inefficiency is that the majority of the added iron is permanently lost to the photic zone, without sequestering carbon to the deep ocean. In contrast, the added nitrogen will stay in the


ocean system until it accompanies carbon to the deep ocean, unless it is lost to one of the processes considered in this paper.

7 Conclusions

A technique is described for calculating the efficiency of carbon sequestration following addition to the ocean of reactive nitrogen in various forms. This technique is used to find values for the various loss mechanisms, both in the ocean and external to the ocean. An important adjustable parameter in the calculations is the maximum chlorophyll concentration that can result from the nitrogen fertilisation. The value chosen for maximum chlorophyll concentration is lower than is routinely observed in the Peruvian upwelling (which leads to a very large and healthy fishery).

The efficiency of the process of sequestering carbon by addition of reactive nitrogen is close to 75% for three selected nutrient types. Although the total loss for each nutrient is similar, the proportion of the loss attributable to ocean causes and to external causes is quite different for nitrate, which has remarkably low oceanic loss, but much larger external loss. In the nitrate case, the positive effect of alkalinity change by photosynthesis is counteracted by the negative of greater carbon dioxide emissions during manufacture.

The overall efficiencies for nitrogen fertilisation are considerably more promising than those achieved with iron fertilisation. They are of sufficient magnitude that fertilisation with nitrogen cannot be ruled out on efficiency grounds. This paper does not address other issues in nitrogen fertilisation, such as cost or environmental effects beyond carbon sequestration.

Acknowledgements

I thank Ian S.F. Jones and Daniel P. Harrison for many stimulating discussions that have helped in developing this paper.

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