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Oceanography Vol.22, No.3236

Ocan

Flaon Scnc, Polc, an Coc

B y A A r O N L . S t r O N g , J O h N J . C u L L e N ,

A N d S A L L i e W . C h i S h O L m

S C i e N C e A N d P O L i C y F e At u r e

ABStrACt. Over the past 20 years there has been growing interest in theconcept o ertilizing the ocean with iron to abate global warming. Tis interest

was catalyzed by basic scientic experiments showing that iron limits primary

production in certain regions o the ocean. Te approach—considered a orm o

“geoengineering”—is to induce phytoplankton blooms through iron addition, with

the goal o producing organic particles that sink to the deep ocean, sequestering

carbon rom the atmosphere. With the controversy surrounding the most recent

scientic iron ertilization experiment in the Southern Ocean (LOHAFEX) and

the ongoing discussion about restrictions on large-scale iron ertilization activities

by the London Convention, the debate about the potential use o iron ertilization

or geoengineering has never been more public or more pronounced. o help

inorm this debate, we present a synoptic view o the two-decade history o iron

ertilization, rom scientic experiments to commercial enterprises designed to

trade credits or ocean ertilization on a developing carbon market. Troughout

these two decades there has been a repeated cycle: Scientic experiments are

ollowed by media and commercial interest and this triggers calls or caution and

the need or more experiments. Over the years, some scientists have repeatedly

pointed out that the idea is both unproven and potentially ecologically disruptive,

and models have consistently shown that at the limit, the approach could not

substantially change the trajectory o global warming. Yet, interest and investment

in ocean ertilization as a climate mitigation strategy have only grown and

intensied, ueling media reports that have misconstrued scientic results, and

conated scientic experimentation with geoengineering. We suggest that it is

time to break this two-decade cycle, and argue that we know enough about ocean

ertilization to say that it should not be considered urther as a means to mitigate

climate change. But, ocean ertilization research should not be halted: i used

appropriately and applied to testable hypotheses, it is a powerul research tool or

understanding the responses o ocean ecosystems in the context o climate change.


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Oceanography Spb 2009 237

1 “LOhA” s hn o “on,” FeX sans o “Felaon Xpn.”

seeking to carry out large-scale ocean

ertilization activities to sell carbon-oset

credits in a carbon trading market. Tese ventures have been a cause o concern

or some scientists and several environ-

mental NGOs, who have argued that

claims o signicant carbon sequestration

are unsupported by scientic evidence,

and that large-scale iron ertilization

will, by design, prooundly alter marine

ecosystems (Chisholm et al., 2001;

Gnanadesikan et al., 2003; Cullen and

Boyd, 2008; Denman, 2008; EC Group

News Release, 2009; World Wildlie Fund

International, 2009). Tese concerns have

helped spur recent UN resolutions, which

were intended to restrict iron ertilization

activities to small-scale scientic research

(UN CBD, 2008; London Convention

Meeting Report, 2008).

As we describe below, the histories o

the scientic and commercial interests

in ocean iron ertilization (OIF) are

intimately connected—co-evolving and

transorming over time. In studying

this history, it becomes apparent that

despite the lack o experimental results

indicating that OIF would be eec-

tive or signicant climate mitigation,

iNtrOduCtiON

Over the 20 years since oceanographer

John Martin o Moss Landing MarineLaboratories quipped, “Give me hal

a tanker o iron, and I’ll give you an

ice age,” ertilization o the ocean with

iron has drawn increasing attention as

a potential geoengineering strategy or

carbon sequestration. As interest in the

idea has increased, so has the contro-

versy surrounding it. In January 2009,

major news services broadcast the

gripping story o the suspension o LOHAFEX1, an iron ertilization

experiment in the Southern Ocean.

Te research vessel Polarstern was

midway between South Arica and South

America when the German Research

Ministry put a halt to the experiment.

Te story was eatured in Wired maga-

zine (Keim, 2009) and on Reuters (Szabo,

2009) and the BBC (Morgan, 2009). A

blog headline covering the controversy

posed the question: “LOHAFEX—I

you mean well, are you allowed to screw

up the oceans?” (Campbell, 2009). Te

experiment drew immediate and intense

commentary rom environmental

nongovernmental organizations (NGOs),

one o which cast it as a violation o the

2008 United Nations (UN) Convention

on Biological Diversity’s moratorium on

iron ertilization activities (EC Group

News Release, 2009). Te international

press, including news articles in Science,

consistently reerred to LOHAFEX as

a “geoengineering project,” an experi-

ment designed to test the potential o

ocean iron ertilization to change global

climate (Kintisch, 2009).

Te LOHAFEX scientists, however,

deended their experiment as purely

scientic and consistent with relevantUN regulations. And, the Director o the

Alred Wegener Institute (AWI), which

sponsored LOHAFEX, deended the

scientic validity o the research, stating

that they “neither plan to nor want to

smooth the way or a commercial use o

iron ertilization with our expedition,”

and that they “oppose iron ertilization

with the aim to reduce CO2

to regulate

the climate” (AWI News, 2009). Aer

the German Research Ministry received

several independent environmental

assessments o LOHAFEX and an impact

statement rom the Indo-German

research crew on Polarstern, the green

light was given (AWI Press Release,

2009a): scientists commenced ertilizing

the Southern Ocean with 10 tonnes o

iron sulate on January 27, 2009.

At the core o the controversy over

LOHAFEX was the idea o using iron

ertilization to mitigate global climate

change by sequestering carbon dioxide

in the deep ocean. Over the last two

decades, this idea has attracted the

interest o several commercial ventures

…the hiStOrieS OF the SCieNtiFiC ANd

COmmerCiAL iNtereStS iN OCeAN irON

FertiLizAtiON (OiF) Are iNtimAteLy

CONNeCted—CO-eVOLViNg ANd

trANSFOrmiNg OVer time.“ ”

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commercial interests have continued to

pursue and advance the idea, ueling a

cycle o media interest, ollowed by calls

or caution, and then proposals or more

research requiring longer and larger

experiments. Here we take a synoptic view o the two-decade history o this

cycle (Figure 1) to better understand

how the scientic and commercial

interests have become intertwined,

conated, and conused. We have much

to learn rom this history, as proposals

or research on other orms o geoen-

gineering are beginning to emerge

(Latham et al., 2008; Rasch et al., 2008).

hiStOry OF PuBLiC-

SeCtOr SCieNtiFiC OCeAN

FertiLizAtiON eXPerimeNtS

t “ion hposs”

While the idea that iron limitation might

control productivity in certain areas o

the ocean has been around since the

mid-1920s (Hart, 1934) i not beore

(de Baar, 1994), the contemporary

history o ocean iron ertilization and the

“iron hypothesis” is attributed to John

Martin. During a 1988 lecture at the

Woods Hole Oceanographic Institution,

Aar L. Sr is Research Assistant,

Department o Civil and Environmental

Engineering, Massachusetts Institute

o Technology, Cambridge, MA, USA.

J J. Cll ([email protected])

is Killam Chair o Ocean Studies,

Department o Oceanography, Dalhousie

University, Haliax, Nova Scotia, Canada.

Salli W. Cisl ([email protected]) is

Martin Proessor o Environmental Studies,

Department o Civil and Environmental

Engineering, Department o Biology,

Massachusetts Institute o Technology,

Cambridge, MA, USA.

F 1. tln o ocan on

laon xpns OiF,

pva sco ns n ,

an polc vlopns.

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F 2. rlaonsp bwn F an CO2

concnaons o

Vosok c cos. Ater Martin (1990b)

Martin amously quipped, “Give me

hal a tanker o iron, and I’ll give you

an ice age” (Martin, 1990a). Reerring

to shipboard experiments on samples

o seawater, and ice core data showing a

relationship between atmospheric irondust deposition and atmospheric CO

2

concentrations over the past 160,000

years (Figure 2), Martin developed a

two-part hypothesis. First, he argued

that the “high nutrient, low chlorophyll”

(HNLC) regions o the ocean could be

explained by iron limitation (i.e., surace

nitrate and phosphate concentrations

were not depleted because additional

phytoplankton growth was limited by iron). Second, he argued that i iron

did indeed control the productivity o

HNLC waters, and thus the transport o

organic carbon to the deep sea via the

so-called biological pump (Figure 3), it

could explain the observed relationship

between atmospheric iron dust deposi-

tion and atmospheric CO2

during the

last glacial maximum (Martin, 1990b).

He also commented that this “paleo-

iron” hypothesis could be important,

because intentional oceanic iron ertil-

ization could prove an eective method

o drawing down atmospheric CO2

“should the need arise” (Martin et al.,

1990; see Box 1).

Using ultra-clean experimental

approaches with seawater incubated on

the deck o a ship, Martin’s team success-

ully demonstrated that iron addition

could stimulate phytoplankton growth

in bottled samples collected rom the

HNLC Gul o Alaska (Martin et al.,

1989) and the HNLC Southern Ocean

(Martin et al., 1990). Wide acceptance o

the iron hypothesis would require tests

on open waters, however. Tough, sadly,

Martin did not live to see it, in 1993 his

colleagues carried out the rst open-

ocean mesoscale (i.e., more than several

kilometers on a side) iron ertilization

experiment, “IronEx I,” in equatorial

Pacic HNLC waters (Figure 4). Te

results demonstrated a phytoplankton

bloom in response to iron addition,

but they were conounded when the

ertilized patch was subducted under

low-density water (Martin et al., 1994).

Tus, several hypotheses remained

untested (Cullen, 1995).

Armed with this experience, a second

experiment, IronEx II, was organized

in May 1995—again in the equatorial

Pacic. Tis time, a 72-km2 patch was

ertilized serially three times over the

course o one week. Tis experiment

demonstrated a strong phytoplankton

response to iron addition in these

HNLC waters, prompting the authors

to conclude that “it is now time to

regard the ‘iron hypothesis’ as the

‘iron theory’” (Coale et al., 1996). Te

authors suggested that the logical next

step was to conduct an experiment in

the Southern Ocean as this is “where

most o the HNLC waters are ound and

where paleoclimate coherence between

iron ux and carbon export has been

observed” (Coale et al., 1996).

t Nx ron o expns:

Cabon Sqsaon

Bcos hposs

Over the ve years rom 1999 to 2004,

eight more major open-ocean iron ertil-

ization experiments would take place in

the Southern Ocean and subarctic Pacic

HNLC regions (Figure 4; able 1). Tese

experiments sought, or the most part,

to track the ate o carbon xed in iron-

induced blooms. As such, they became

increasingly ocused on the question o

carbon export rom the surace waters,

as this is what is necessary to draw CO2

out o the atmosphere and transport it

into the deep sea. At the same time, as

interests in OIF or carbon sequestra-

tion were taking o (see below), the

scientic language began to morph:

increasingly, “carbon export” became

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“carbon sequestration” (Boyd et al., 2000,

2004; Buesseler et al., 2004), a term

used in the US Department o Energy

(DOE) climate mitigation vocabulary

(Department o Energy, 1999). Tis

shi in language contributed to blurring

the lines between the basic and applied

science dimensions o OIF.

An analysis o the “post-IronEx”

mesoscale experiments illuminates the

evolution o hypotheses that motivated

them (able 1; see de Baar et al., 2005,

and Boyd et al., 2007, or reviews). Te

new ocus on the Southern Ocean began

with the Southern Ocean Iron Release

Experiment (SOIREE) and the European

Iron Enrichment Experiment (EisenEx;

Boyd et al., 2000; Smetacek, 2001),

and placed more emphasis on longer-

duration experiments tracking particle

export, remineralization, and changes in

zooplankton communities. Both experi-

ments conrmed the hypothesis o iron

limitation o primary production in

the HNLC Southern Ocean. Although

diatom production increased in response

to iron addition in the SOIREE patch,

carbon export did not (Boyd et al., 2000).

EisenEx also demonstrated a diatom

bloom, and measured a larger net atmo-

spheric CO2

drawdown than SOIREE,

but storms interrupted the experiment

and the ate o xed carbon could not

be tracked (Assmy et al., 2007). A year

later, SEEDS-I (Subarctic Pacic Iron

Experiment or Ecosystem Dynamics

Study) conrmed that productivity

was limited by iron in the HNLC

region o the western subarctic Pacic,

F 3. Cabon ox a wol

ows b n aosp s

so n p sa bcas

bolocal pp ps an kps

. Poplankon n l

sac la ak p nns

.., na an pospa an

ow, convn CO2 o oanca a ls an oo wbs.

So o oanc ao

xapl, snscn poplankon,

cal plls, an aa bs

snks o p ocan w

coposs, lasn CO2

an

nns wl consn oxn.

Wn ocan cabon ccl s

ol n balanc, s cabon an

nnc p wa os no

ac sac o cas o

ns o as, an wn os,

bolocal pocv conss

CO2 an nns an sns C, N,an P back o p was as snkn

oanc a. T aon o CO2

s so n p sa lal

cospons o aon o ajo

nns N an P cons n

l sac la o ocan.

Wn on ls pocv, N an

P pss w woln’ o

ws; on laon s allva,

ajo nns a cons, o

oanc a s poc, an o

cabon snks o p sa. Ts xa cabon assoca w a on naal o nnonal

col b cons sqsaon. B aon an aon o cabon sqsaon pns on ow

p oanc a snks bo s copos an w o no on s sll avalabl n xcsswn cabon an nnnc was ac sac aan. Figure modifed rom Chisholm (2000)

8/8/2019 22 3 Strong



documenting a oristic shi toward

diatom production. Carbon export was

not measured (suda et al., 2005).

Te next set o experiments were

designed to be larger and longer, with

the hope that this would allow better

tracking o the ate o iron-induced

blooms. Te Southern Ocean Iron

Experiment (SOFeX), a multi-part,

multi-ship iron ertilization expedi-

tion, set out to address hypotheses

about carbon export as inuenced by

silicate availability in the context o

iron-induced blooms (Coale et al., 2004).

SOFeX produced the rst conclusive

measurement o enhanced particulate

organic carbon (POC) export resulting

rom an intentional iron-ertilization-

induced bloom (Buesseler et al.,

2004). Although POC export rom the

iron-enriched patch was elevated, the

incremental ux was small compared

to those observed during a natural iron

ertilization event in the same location

in 1998 (Buesseler et al., 2001). Te

authors concluded that the observed

carbon ux was small relative to what

would be required by proposed geoengi-

neering plans to sequester carbon using

iron ertilization, but they stressed that

they had not been able to observe the

termination o the iron-induced bloom

(Buesseler et al., 2004).

Te Subarctic Ecosystem Response

to Iron Enrichment Study (SERIES)

expedition ollowed. Conducted over a

month in the subarctic Pacic, a 77-km2

iron-enriched patch was created and

POC export ux monitored (Boyd

et al., 2004). Te decline and termina-

tion o the iron-induced bloom (caused

by silicate limitation) was observed.

Te majority o the carbon xed in

SERIES was remineralized by bacteria

and zooplankton grazing in the surace

waters. Only a small raction (8%) o

the xed carbon sank below the 120-m

permanent pycnocline, signicantly

lower than the deep-export rate observed

in natural blooms (Buesseler, 1998).

Further, the iron content (Fe:C) o the

exported material was a thousandold

higher than that assumed in assess-

ments o the efciency and cost o OIF

or climate mitigation. Noting increased

attention to the idea o iron ertilization

or geoengineering, Boyd et al. (2004)

argued that “inefcient vertical transer

o carbon may limit the eectiveness o

iron ertilization as a mitigation strategy.”

Te European Iron Fertilization

Experiment (EIFEX), conducted in

2004 and the longest iron ertilization

experiment to date, was also designed to

evaluate the carbon export response and

community shis in a Southern Ocean

iron-induced bloom (Homann et al.,

2006). Biomass export resulting rom

the sinking o an iron-induced bloom

represented the highest ratio o carbon

exported to added iron to date (Jacquet

et al., 2008). At the same time, SEEDS-II

a second subarctic Pacic experiment,

detected no signicant bloom response

to iron enrichment (suda et al., 2007).

Box 1. T PaloCla Poon o ion hposs: Sll an Opn Qson

rcnl, so palocanoaps av call no qson casal lnk bwn aospc s poson an low aospc CO2

an s a cool cla n las lacal ax. Kol al. 2005 anal ol o bolocal pp n lacal CO2

aw

own sn sn cos, o xapl. T aa nca a n la poons o Son Ocan, xpo pocv was acall

low n las lacal axxacl n a po o ncas s x. T s a a on laon o s col

no av bn soll sponsbl o CO2

awown Kol al., 2005.

usn s pocv aa an os o os Paan al., 1996; Anson al., 2008 an copan o s x cos o

Wnckl al. 2008, Anson al. 2007 psn an an a s no colaon n palocanoapc aa bwn s

x an ncas xpo pocv n qaoal Pacfc o Son Ocan. Wl aa o sow a son ancolaon

bwn s x an CO2 , a a s no vnc a s cas CO

2awown. T casal n o

onal c co aa F 2 as bn a cnal a n an o OiF o onnn, an, a v las, s cn a

ns qsonn a casal sv o anon an sac Anson al., 2007. Alna poss ncl son nncs

o cann wn pans on ovnn o cabonc son p wa towl al., 2006.

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wo other experiments were

conducted in 2004 to test additional

biogeochemical hypotheses using

iron enrichment. Te Surace-Ocean

Lower-Atmosphere Studies Air-Sea Gas

Exchange (SAGE) experiment in the

sub-Antarctic Pacic o New Zealand

sought to understand the eects o iron

addition on air-sea gas exchange, partic-

ularly dimethylsulde (DMS). DMS

plays a role in cloud ormation, and as

such is thought to play a role in climate

regulation and, potentially, in increasing

Earth’s albedo (Charlson et al., 1987).

In this experiment, scientists ertilized

serially with over 5 tonnes o iron sulate,

but ound only a modest chlorophyll

increase and no increase in either CO2

drawdown or DMS production, which

they believed may have been due to light

limitation (Law et al., 2006). Another

iron-enrichment experiment, FeeP,

perormed a combined Fe and phosphate

addition to low nutrient, low chloro-

phyll (LNLC) waters in the Northeast

Atlantic to test the hypothesis that iron

enrichment o LNLC waters can lead to

a net N import (ultimately supporting

increased productivity) by stimulating

nitrogen xation. Although rates o

nitrogen xation increased in response

to enrichment, productivity did not.

Carbon export in response to enrich-

ment was not measured (Rees et al.,

2007; Karl and Letelier, 2008).

Collectively, these experiments taught

us a good deal about the initial phyto-

plankton community response to iron

enrichment, and conrmed iron limita-

tion o productivity in HNLC regions

around the globe. Te results, however,

were highly variable and inconclusive

with regard to carbon sequestration: the

major conclusion to be drawn is that

physical oceanographic, geographic, and

biological variability all inuence the

long-term ate o blooms induced by iron

ertilization, signicantly constraining

generalizations about iron-induced

carbon sequestration (Boyd et al., 2007).

moln

Open ocean iron enrichment experi-

ments over the last 16 years have

conrmed the hypothesis o iron limita-

tion o productivity in HNLC regions

and have provided evidence or highly

F 4. Locaons o ajo afcal on ncn xpns, ncln plo onsaons o gnSa Vn

an Plankos. Colo a ap psns sac na concnaons w wa colos ncan concnaons,

sown ajo hNLC ons n Son Ocan, asn qaoal Pacfc, an sbacc Pacfc. Data rom

National Virtual Ocean Data System, http://erret.pmel.noaa.gov/NVODS/; analyzed nitrate data rom the World Ocean Atlas 2005

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variable, and small, rates o carbon export

rom these iron-induced blooms. But

experiments at this scale cannot resolve

key questions about geoengineering

scenarios or carbon sequestration on

the order o decades to centuries, and onthe scale o the entire Southern Ocean

and beyond. Tese questions can be

addressed eectively only by using global

biogeochemical models.

From the very beginning o research

on the iron hypothesis, models were used

explicitly to predict what small-scale

experiments could not show: the global

carbon cycle response to large-scale

OIF. In response to the initial interestin iron ertilization as a potential tool

or global climate mitigation in 1990,

Sarmiento and Orr (1991) modeled

what complete depletion o surace-layer

macronutrients in the Southern Ocean

(by iron-induced phytoplankton blooms)

would do to global atmospheric CO2

and

ocean chemistry. Teir model, operating

on a 100-year time rame, predicted

a net global drawdown o around

1–1.5 Gt C yr-1 (98–181 Gt C total over

100 yr). At the time, this gure repre-

sented osetting about 20% o anthro-

pogenic emissions over the 100 years,

corresponding to a delay in the rising

atmospheric CO2

trajectory o about

18 years. Even so, the projections resulted

in a global atmospheric concentration o

CO2

near 700 ppm by 2100. Teir model

also predicted a huge area o anoxia in

the southwestern Indian Ocean, and a

high potential or methane production

as a result o this anoxia (Sarmiento and

Orr, 1991; see also Fuhrman and Capone,

1991). O essential importance is that

these results, by design, represent the

extreme (unrealistic) case scenario—

ertilizing the entire Southern Ocean

with iron or 100 years, and assuming

that all o the macronutrients available

were completely used up. Tus, these

results represent an unachievable (both

logistically and ecologically) upper limit.

Since these initial modeling eorts,there have been many published

variations on the theme (able 2)—all

concluding, more or less, that large-

scale ocean ertilization could, at the

limit, sequester only modest amounts o

carbon relative to global human emis-

sions. All such scenarios involve spatial

scales o the entire Southern Ocean or

beyond and time scales o decades to

centuries. Most recently, Zahariev et al.(2008) modeled how the “elimination

o iron limitation” in the ocean globally

would aect atmospheric CO2. Teir

results were similar to previous esti-

mates: rates o 0.9 Gt C yr-1 reduction

in atmospheric carbon, or about 11% o

2004 global emissions, and these seques-

tration rates could only occur “or a year

or two, even under continuous ertiliza-

tion.” Tey conclude that their idealized

model o iron ertilization oers only

a “minor impact on atmospheric CO2

growth” (Zahariev et al., 2008).

Te early publications also recognized

the downstream eects o OIF, that

is, (1) the inuence o iron-induced

nutrient depletion on surace waters

that are subducted and transported,

and that ultimately resurace elsewhere

with diminished nutrient supplies, and

(2) enhanced decomposition o organic

matter in subsurace waters, depleting

oxygen with ecological and biogeochem-

ical consequences that over time will

extend well beyond the ertilized loca-

tion. As Sarmiento and Orr (1991) put

it, the act that an increase in produc-

tivity o such a magnitude would be

concentrated in 16% o the world ocean

would have “dramatic eects on oceanic

ecology which are difcult to predict.”

Fuhrman and Capone (1991) high-

lighted expected inuences o enhanced

nutrient cycling on global productiono the potent greenhouse gases methane

and nitrous oxide. Including tenta-

tive assessments o eects on sheries,

Gnanadesikan et al. (2003) modeled

what some o the long-term downstream

ecological eects o nutrient depletion

might look like, and argued that down-

stream reduction in productivity could

ar outweigh the benet o the initial

iron-induced carbon sequestration interms o a global carbon budget.

In short, marine ecosystems are

complex, and any estimate o the net

impact o iron ertilization on global

carbon storage and greenhouse warming

requires an analysis o all o the down-

stream potentially negative eects,

including a long-term reduction in ocean

productivity, alteration o the structure

o marine ood webs, and a more rapid

increase in ocean acidity (Denman,

2008). As argued by Cullen and Boyd

(2008), such long-term and downstream

eects must not only be acceptably

predictable, but also veriable, i OIF is

to be considered a viable technology or

climate mitigation. So ar, no proponents

o OIF have demonstrated, or even

argued, that these eects can be moni-

tored over decades to reveal statistically

signicant assessments against the back-

drop o climate variability.

inan Scnc

an movn Fowa

Between 2005 and 2009, the scien-

tic community reviewed the results

rom previous articial ertilization

8/8/2019 22 3 Strong



experiments and models (de Baar

et al., 2005; Boyd et al., 2007; Powell,

2007–2008) and began a more public

discussion about where the eld was, and

should be, going (Boyd, 2008; Buesseler

et al., 2008; Lampitt et al., 2008; Smetacek

and Naqvi, 2008). Although mesoscale

experiments had shown that iron addi-

tion caused phytoplankton blooms in

HNLC regions, what happened to the

carbon in those blooms, however, was

less consistent and did not support key

calculations in Martin’s “paleo”-iron

hypothesis. For example, an analysis

o results rom experiments in the

Southern Ocean (de Baar et al., 2005)

revealed that the average net dissolved

inorganic carbon (DIC) drawdown

rom the atmosphere as a result o

iron enrichment was approximately

4347 mol C per mol Fe. Assuming a

carbon export rate to the deep ocean

o 20% o primary production, carbon

export efciency (amount o carbon

exported to the deep ocean per unit o

iron added) is thus 870 mol C per mol Fe.

Tis gure is 200 times less than required

to explain paleo-climate observations

(de Baar et al., 2005). Tus, the collective

carbon export efciency results rom

open-ocean experiments were signi-

cantly lower than initially hypothesized.

An important symposium was held

at the Woods Hole Oceanographic

Institution (WHOI) in September

2007 (http://www.whoi.edu/page.

do?pid=14617) that included invited

representatives o private companies

promoting ocean ertilization or climate

mitigation. Experimental results and

modeling predictions, as well as the

policy implications and economics o

OIF, were discussed. In an outgrowth

o that workshop, Powell (2007–2008)

summarized the state o OIF science

as it relates to climate mitigation. He

concluded that iron ertilization may

work in principle to sequester some

carbon, but yields are low and long-

term sequestration is difcult to veriy,

making it less attractive and making

the cost per ton o carbon seques-

tered greater than proponents might

hope. Uncertainties about ecosystem

tabl 2. Slc ols o lascal ocan on laon an s pac on aospc cabon nvno.

mos ols sow as o CO2

awown n sac was, w onl a sall acon xpo blow pcnocln, an onl a sall acon o a xpo cabon sqs. mols conv a < 1g C 1 , an

nall ass naconsan laon o vas hNLC aas o cas o cns.

Model Approach

Overall estimate

of C sequestered

Maximal estimate of

C sequestration rate Summary

Sano anO, 1991

Copl aconn plon o on laon o hNLC ons

98–181 g C ov 100 s

ras aon1–1.5 g 1 na ova cn

Asss copl aconn plon oOiF o n Son Ocan an sls n a 20%con n anoponc ssons onl s lvlo laon s anan o 100 as.

gnanaskan al., 2003

Pac laon;ncls ownsaeects of macronun plon onbolocal pp

ulal, naveect on productivity

o OiF col b30x aon o Cxpo o OiF

2–20% sqsaon o 2 g 1 asan nal sao lobal xpopocon

Sqsaon o 100 s a sall pcnao annal xpo pocon. Ovall ownsa pacs o OiF a ow cabonsqsaon spons.

Aon anBopp, 2006

uss ols bas onOiF xpns osla pocv,

xpo pocon, anlal sqsaon

70 g C ov 100 s

expo pocon:inal ncas3.8 g 1 , slowso 1.8 g 1

Sqsaon:0.3–1 g 1

ulal, 90% o sqsaon cos o Son Ocan. mol pcs sbsanal ncass npocv. Onl a acon o s pocv s l

al xpo, an onl a acon o a s lalsqs. rqs consan s laon.

Jn al., 2008

mols pac o basnscal laon oon ca; analsCO

2awown

3.4 g C ov 10 s N/A

T ol sows aospc CO2

uptake eciency, but low total biological pump eciency: full

laon o n Pacfc hNLC o 10 s slsn 3.4 g o CO

2awown.

zaav al.,2008

Copl l o onlaon n lobalocan

77 g C ov 5,300ax

1 g 1 axConnos laon o n Son Ocanresults in about 11% oset of global emissions under the

os al conons.

8/8/2019 22 3 Strong



disruption and other potential down-

stream negative side eects were also

recognized as a cause or concern.

In an outgrowth o the WHOI

workshop and in an eort to move the

eld orward, Buesseler et al. (2008)ocused on the need to reduce uncertain-

ties about OIF as a climate mitigation

strategy, arguing that there is “as yet, no

scientic evidence or issuing carbon

credits rom OIF.” Tey urged a move to

larger and longer experiments because

“ecological impacts and CO2

mitigation

are scale-dependent” (Buesseler et al.,

2008). Te proposed experiments would

seek to test a broad array o ecosystemimpacts o iron ertilization, would inte-

grate with modeling eorts to analyze

potential downstream eects o OIF, and

would attempt more detailed measure-

ments o the ate o xed carbon rom

iron-induced blooms.

Around the same time, Smetacek and

Naqvi (2008)—arguing that an apparent

consensus against OIF was premature—

also called or larger and longer experi-

ments to test both the geoengineering

potential o OIF and the potential

or unintended negative side eects.

Collectively, these proposals advocated

cautiously moving orward, gradually

increasing the size o experiments, and

measuring carbon export, net green-

house gas budgets, ood-web disruption,

and other parameters, in order to gain

more inormation about the potential o

iron ertilization as a climate mitigation

strategy. Following up on arguments

presented at the WHOI workshop,

Cullen and Boyd (2008) pointed out that

it will be necessary to predict and veriy

cumulative and long-term eects o OIF

or climate mitigation, and there are

good reasons to believe that it may not

be possible to detect signicant down-

stream eects o wide-scale OIF, such as

increased anoxia and nitrous oxide emis-

sions, against a background o ocean

variability. It ollows that i negative

eects were large but masked by natural variability, they might not be detectable

until they were irreversible. But regard-

less, it was the responsibility o propo-

nents to show that these eects could be

assessed (Cullen and Boyd, 2008).

As the cycle o experimentation,

media coverage, and calls or more

research on unintended side eects

continued, the scientic questions being

addressed by OIF experiments evolvedsubstantially. One dening aspect has

emerged: the experiments that were once

ocused on controls o ocean produc-

tivity and their relationships to climate

are now almost exclusively couched—

either explicitly or implicitly—in terms

o testing iron ertilization as a carbon

sequestration strategy or mitigating

excess global atmospheric CO2.

Te rst experiment aer the 2008

calls or geoengineering research,

LOHAFEX, was conducted in early

2009 amidst international controversy

and aer a temporary suspension by the

German government. Te controversy

stemmed rom a belie that the experi-

ment, the largest and longest conducted

to date, would pave the way or geoengi-

neering projects and, by being an experi-

ment designed to test the idea that iron

ertilization could alter CO2

concentra-

tions, was itsel geoengineering.

Te initial results o the LOHAFEX

experiment, conducted over 40 days

using 10 tonnes o iron sulate distrib-

uted over 300 km2, demonstrated the

expected iron-induced bloom (AWI

Press Release, 2009b). However, the

bloom also induced an increase in

copepod grazing and amphipod abun-

dance, channeling carbon into the ood

web and largely to respiration; in this

way, the vast majority o the newly

xed carbon was rapidly remineral-ized and only a negligible amount was

exported. Te National Institute o

Oceanography (NIO) report indicated

that these results “dampened the hopes”

o using OIF in the Southern Ocean to

mitigate global climate change (NIO

Press Release, 2009). Te controversy

surrounding LOHAFEX brings into

ocus the dynamics between OIF science,

companies hoping to conduct OIFcommercially, and international and

national regulations on OIF. No publicly

unded scientic experiments beyond

LOHAFEX have been announced, but

uture experiments will be conducted

under new regulatory regimes and,

certainly, under close scrutiny.

OCeAN FertiLizAtiON AS A

COmmerCiAL VeNture

t hso o Cocal

ins Paallls Scnc

As the iron hypothesis—and John

Martin’s amous quip—became popular-

ized, so did the idea that ertilizing the

ocean could be a cheap, ast, and easy

solution to the greenhouse gas problem.

Not long aer the hypothesis was rst

put orward, Te Washington Post

published an article on iron ertiliza-

tion as way to “battle the greenhouse

eect” (Booth, 1990). Tis attention

would quickly translate into commercial

ventures seeking to prot rom ocean

ertilization’s geoengineering potential.

Aer the rst round o press coverage,

the American Society o Limnology and

Oceanography (ASLO) held a workshop

8/8/2019 22 3 Strong



to review the science (ASLO, 1991).

Aer many presentations and long

discussion, participants agreed on a reso-

lution, endorsed by the Society, “urging

all governments to regard the role o

iron in marine productivity as an areaor urther research and not to consider

iron ertilization as a policy option that

signicantly changes the need to reduce

emissions o carbon dioxide” (see preace

to Chisholm and Morel, 1991). Tis

resolution’s emphasis on the scientic

uncertainties surrounding the ecosystem

response to iron ertilization stimulated

important OIF research as intended,

but the careully worded phrase aboutOIF as a policy option did not stem the

growing interest in ocean ertilization or

commercial gain.

Interested in what appeared to be

an easy and intriguing solution or

global warming, the press ollowed the

IronEx I and II experiments in 1993

and 1995, and interpreted their results

in a dierent context rom the intent o

the experiments. Te addition o iron

to equatorial Pacic waters in IronEx I

resulted in a phytoplankton bloom, and

the scientists involved were justiably

very excited about the results: iron did

indeed stimulate the growth o phyto-

plankton consistent with the rst arm

o the iron hypothesis—that iron limits

productivity in these HNLC waters. Te

magnitude o the bloom, however, was

muted, in part because o the design,

and in part because o unexpected

physics during the experiment. Te press

coverage o the experiments, however,

ocused on the small magnitude o the

bloom and its meaning in the climate

mitigation context, rather than the

exciting act that there was a bloom

at all. (Tis view is understandable, as

they are writing or an audience that is

not interested in whether or not iron

limits HNLC regions o the ocean; it is

interested in climate change.) One head-

line prompted by the low-magnitude

response during the IronEx I experimentread: “Pumping iron: too weak to slow

warming” (Monastersky, 1994), and

another account reported that “the idea

o ertilizing the entire Southern Ocean

should probably be considered dead”

(Kunzig, 1994). But such skepticism was

short-lived. When results rom IronEx II

were published in 1996, Te Washington

Post ’s coverage described them as a

conrmation o Martin’s hypothesis o

CO2

sequestration and climatic cooling

(Suplee, 1996).

t Fs Cocal

Poposal: Ocan Flaon

o Fs Pocon

In 1994, beore IronEx II had taken

place, Michael Markels Jr., ormer CEO

o the engineering rm Versar Inc., led

the rst o several patent applications

or a method o improved production o

seaood by ocean ertilization (Markels,

1995). Te method reerred to ertilizing

with “all nutrients that are ound to limit

production in the surace ocean.” In this

patent, Markels cited the results o the

IronEx I experiment and suggested that

he could constantly ertilize 140,000 km2

o the Gul Stream (which is not an

HNLC region) with enough iron, phos-phate, and micronutrients to remove

1.3 Gt o CO2

and produce 50 Mt o

additional seaood production annually

(Markels, 1995).

Markels would go on to ound Ocean

Farming Inc., a company seeking to capi

talize on what it said was ocean ertiliza-

tion’s promise to increase sh biomass

production. In early 1998, Ocean

Farming Inc. carried out two successive

small-scale (9 km2) ocean iron ertiliza-

tion “demonstrations” in the Gul o

Mexico. Te results were not published,

but it was reported that, while the iron

ertilization induced an initial increase

in phytoplankton production, the bloom

ailed to expand as much as anticipated,

owing to a “second limitation,” most

likely rom phosphorus (Markels and

Barber, 2001)—an unsurprising result

because the Gul o Mexico is a low

macronutrient region, not avorable

to iron-induced bloom development

(Markels and Barber, 2001).

We SuggeSt thAt it iS time tO BreAK thiS

tWO-deCAde CyCLe, ANd Argue thAt We KNOWeNOugh ABOut OCeAN FertiLizAtiON tO SAy thAt

it ShOuLd NOt Be CONSidered Further AS A meANS

tO mitigAte CLimAte ChANge.“”

8/8/2019 22 3 Strong



Citing its own unpublished activities

rom the Gul o Mexico, and the initial

results rom IronEx I and II experiments,

Ocean Farming Inc. then reportedly

secured a lease o 800,000 square miles

o LNLC tropical ocean in the exclusiveeconomic zone o the Republic o the

Marshall Islands in the western Pacic

Ocean (Markels, 1998). According to the

structure o the lease, once ertilization

o this vast area occurred and sh catch

had commenced, Ocean Farming Inc.

would pay the Marshallese government

$3.75 a square mile or 7% o the prot,

whichever was more (Markels, 1998).

t Can o Cabon Cs

While the ertilization o the waters

near the Marshall Islands never did take

place, the idea o commercializing the

ecosystem response to ocean ertilization

did not disappear. Instead, it morphed.

As Markels wrote in 1998, “Ocean

ertilization also promises benets that

should be welcomed by those concerned

about possible global warming. Te

growth o phytoplankton in the ocean

removes CO2, a greenhouse gas, rom

the ocean surace and the atmosphere.

About hal o the carbon removed in

ertilized areas will sink to the bottom o

the deep ocean…Te continuous ertil-

ization o the same 100,000 square miles

o tropical ocean should sequester about

30 percent o the CO2 produced by theUnited States rom the burning o ossil

uels” (Markels, 1998). Tis statement

was published beore any OIF experi-

ment had provided an estimate o carbon

export rom an iron-induced bloom. A

year later in an article in the journal o

the Cosmos Club, Markels discussed

combining the dual purposes o ocean

arming and carbon sequestration rom

OIF. He also started a new company,

GreenSea Venture, which sought to

commercialize ocean ertilization to

sell carbon oset credits or seques-

tered CO2

(Markels, 1999).

A mo Cow Fl: gnSa

Vn gs a Copo

In the late 1990s, a second corporation

seeking to invest in ocean iron ertiliza-

tion as a way to sequester carbon and sell

carbon oset credits, Carboncorp USA,

was created. According to an archived

copy o the Carboncorp USA Web site

(Carboncorp USA, 1999), “Ocean

Carbon Sequestration (OCSM) patented

nutrient supplements will stimulate an

immediate plankton bloom. Tis bloom

o plant biomass removes CO2

rom the

atmosphere and stores it saely in richphytoplankton.” At the time, Carboncorp

USA proposed to use commercial ships

traversing shipping lanes on the high

seas to meter small amounts o the

company’s nutrient supplements into the

water. Te idea was to oset the emis-

sions o the shipping by sequestering

carbon and selling credits (Carboncorp

USA, 1999; Adhiya, 2001).

By 2001, Carboncorp USA haddisappeared, and many o its ideas were

presented by Ocean Carbon Sciences

Inc., led by Vancouver-based entrepre-

neur Robert Falls. Representatives rom

both Ocean Carbon Sciences Inc. and

GreenSea Venture were invited partici-

pants in a 2001 ASLO workshop on iron

ertilization (ASLO Workshop Statement,

2001), as commercial ocean ertilization

or carbon sequestration was attracting

attention and investment (Krivit, 2007).

Scaln up: A Poposal Fo a

tcnolo donsaon

Ocean Carbon Sciences Inc. initially

committed $325,000 CAD to the

Canadian component o the SERIES

experiment, but deaulted on the pledge,

did not participate in the experiment

(Canadian SOLAS Report, 2003), and

made little headway toward conducting

its own experiment. GreenSea Venture,

however, was moving orward. In 2001,

Michael Markels teamed up with Richard

Barber, a highly respected biological

oceanographer at Duke University

and one o the scientic team rom the

original IronEx experiments. At the 2001

But, OCeAN FertiLizAtiON reSeArCh ShOuLd

NOt Be hALted: iF uSed APPrOPriAteLy ANd

APPLied tO teStABLe hyPOtheSeS, it iS A POWerFuL

reSeArCh tOOL FOr uNderStANdiNg thereSPONSeS OF OCeAN eCOSyStemS iN the CONteXt

OF CLimAte ChANge.“ ”

8/8/2019 22 3 Strong



National Energy echnology Laboratory

Conerence on Carbon Sequestration,

hosted by the Department o Energy,

Markels and Barber announced plans

or GreenSea to move ahead with a

5,000-square-mile “technology demon-stration” o ocean iron ertilization or

carbon sequestration in the HNLC

region o the equatorial Pacic (Markels

and Barber, 2001). Supporting their

proposal, they cited the two IronEx

experiments, SOIREE, and Ocean

Farming’s two Gul o Mexico demon-

strations. Although none o these experi-

ments showed any carbon export rom

an iron-induced bloom, it was arguedthat increasing the size o the ertilized

patch approximately 100 times rom

previous experiments would yield better

estimates o carbon export potential o

OIF (Markels and Barber, 2001). While

the proposed technology demonstration

never did take place, the commercial

potential suggested in their proposal—

quoted at a cost o $2 per ton o seques-

tered carbon dioxide, including the cost

o verication, overhead, and prot—

served to broaden the discussion about

the ways in which ocean ertilization

experimentation should move orward.

Despite no direct scientic evidence

that ocean ertilization could substan-

tially slow global warming, the simply

stated appeal o OIF as a quick climate

x continued to attract media attention.

Tis attention, in turn, urther ueled

commercial interest in the idea. In an

interview with Wired magazine in 2000,

Markels claimed that “given 200 boats,

8.1 million tons o iron, and, say, 11

percent o the world’s ocean,” he could

“zero out global warming. Next ques-

tion?” (Graeber, 2000). Te vision o

commercial ventures interested in using

iron ertilization or geoengineering was

unquestionably large in scope and was

not being dictated by the results o initial

scientic OIF experiments.

Scnss gv mx SnalsAt this point, the activities o GreenSea

Venture and Ocean Carbon Sciences

elicited a response rom oceanographers,

who raised concerns about the discon-

nect between scientic evidence and

commercial proposals. Several o us cited

the difculties o veriying the magni-

tude o carbon sequestration explicitly

caused by ocean iron ertilization, and

argued that this would make oceanertilization ineligible or carbon credits

(Chisholm et al., 2001). We pointed

out urther that widespread ecosystem

disruption is inherent to the design o

ocean ertilization, and the unintended

consequences o this disruption would

likely be signicant and unpredictable.

Although we maintained that ocean iron

ertilization should not be conducted

on a commercial scale, we also made

explicitly clear that we were not arguing

against small-scale scientic iron enrich-

ment experiments designed to answer

specic questions about how marine

ecosystems unction. Some elt that we

had “overstated the current knowledge

in reaching [our] opinion that iron

ertilization is not a viable option or

CO2management” (Johnson and Karl,

2002), and countered that veriying

carbon credits is not the critical issue,

what is key is whether OIF “is a easible

strategy to mitigate increasing CO2

in

the atmosphere” (Johnson and Karl,

2002). Tus, the potential or climate

mitigation using OIF was gaining cred-

ibility (at least as a testable hypothesis) in

the scientic community.

the reCeNt hiStOry OF

COmmerCiAL OiF ANd OiF

reguLAtiON

Cocal Vns

Conn o expn

As scientists were gearing up or theSOFeX experiment in the Southern

Ocean, Caliornia-based entrepreneur

Russ George ounded the Planktos

Foundation, which billed itsel as a

not-or-prot organization seeking to

use iron ertilization to solve global

warming. Planktos oered, or sale by

charitable donation on the Internet,

$4 “Green ags” (Planktos Green ags,

2002), which were in eect like personal,small carbon ootprint osets and would

be used to support the oundation’s

eorts to develop iron ertilization as

a technology or carbon sequestration

(Plotkin, 2002).

In the summer o 2002, temporally

and geographically between SOFeX in

the Southern Ocean and SERIES in the

Gul o Alaska, the Planktos Foundation

conducted its own iron ertilization

“demonstration,” dumping iron-

containing paint pigment into the North

Central Pacic along a 50-km transect

east o Hawaii (not HNLC waters)

rom Neil Young’s antique sailing yacht,

Ragland (Schiermeier, 2003). Journalist

Wendy Williams quoted Russ George

in a piece or Living on Earth as arguing

that this ertilization project had induced

a large phytoplankton bloom and had

sequestered enough carbon to oset the

entire carbon ootprint o his Caliornia

hometown o Hal Moon Bay. George

urther described Planktos’ activity as

“really more o a business experiment”

(Williams, 2003). Although the results

o the experiment were never made

public, a description o the activity was

8/8/2019 22 3 Strong



published in the news eature section o

Nature the ollowing year (Schiermeier,

2003), including a photo o George on

Ragland . Te Planktos Foundation, and

the entire idea o carbon credit sale rom

ocean ertilization, was gaining attention

and momentum.

Lal isss As

As it became evident that commercial

operations were moving orward,

concerned scientists and environmental

groups continued to raise questions

about the efcacy and legality o

commercial ocean ertilization. Tere

appeared to be no law preventing

ocean ertilization beyond the 200-mile

exclusive economic zone o any country

(Markels and Barber, 2001; McKie,

2003). Indeed, to our knowledge, the

initial, small-scale, scientic OIF experi-

ments were carried out without permits,

as there were no clear statutes at the

time. Also, it was widely recognized

that the small scale o the experiments

rendered their impacts miniscule and

ephemeral by any measure.

Several international treaties cover

activities in international waters,

including the United Nations Convention

on the Law o the Sea, the 1972 London

Convention on Marine Pollution and

Ocean Dumping, and the 1959 Antarctic

reaty, which covers portions o the

Southern Ocean. Te UN Convention

on Biological Diversity also regulates

activities that will impact ecosystem

species diversity (see Boxes 2A, 2B, and

2C). At a 2001 ASLO workshop on ocean

ertilization, the ormer secretary o

the Intergovernmental Oceanographic

Commission, Geo Holland, stated

that “there are no legal precedents that

apply directly to ocean ertilization,

though there are parts o existing laws

that are relevant” (Holland, 2001). At

the time, it was not clear whether ocean

ertilization ell under the purview o

the London Convention, and the lack

o clarity on the legal issue meant that

commercial interests could move ahead,

or the time being.

Cocal Vns Avanc

Plans o Flaon as Scnss

dba is F

Aer 2004, while scientists were

analyzing previous results and planning

uture experiments, commercial interests

continued to advance their plans. Te

Box 2A. un Naons Convnon on Law o Sa uNCLOS

WhAt:

• International treaty rst passed in 1982 that governs territorial legality of the ocean areas.

• United States has not yet ratied it, but many provisions are regarded as binding international law.

• Te Law of the Sea sets limits for exclusive economic zones and laws of conduct on the high seas.

• UN General Assembly passes relevant resolutions. UN’s International Maritime Organization and other organizations administer UNCLOS.

hoW It ReLAteS to oIF: Sval nal povsons o uNCLOS a lvan o OiF. Acl 145 splas a s o sas o an

scnfc sac s b o pacl pposs a owa ncas o knowl an nsann o all ankn. Vaos

o acls oln qns o sas o poc l o an nvonn. uNCLOS s also lvan o OiF o fs pocon, as

ovns bo laon o fsn s wn xclsv conoc ons eezs an fsn s on sas.

Key StAtementS And deCISIonS on oIF:

Dec 2007: General Assembly resolution calls for more research into the eects of ocean iron fertilization.

dc 2008: gnal Assbl solon wlcos Lonon Convnon an Convnon on Bolocal dvs

csons aans lascal OiF.

FutuRe ReguLAtIonS: Alo gnal Assbl as no pass spcfc lao solons an OiF, cnal o

uNCLOS o a laon, an s lvanc o nvonnal pocon, scnfc sac laon, an nnaonal was lal

sss, col ak a oo o o coona laon o on laon n .

8/8/2019 22 3 Strong



Planktos Foundation became Planktos

Inc. in 2005 and was shortly thereaer

purchased by Solar Energy Limited

(Business Wire, 2005a). Later that year,

Diatom Corporation agreed to purchase

the marketing rights or carbon credits

generated rom Planktos Inc.’s iron

ertilization activities (Business Wire,

2005b). About 18 months later, publicly

traded Diatom Corp. became Planktos

Corp. (Business Wire, 2007). During

this time, the other commercial entity

involved in OIF, GreenSea Venture,

had moved rom ocean ertilization

demonstrations to nancial support or

Box 2B. Convnon on Pvnon o man Pollon b dpn o Wass

an O ma 1972 Lonon Convnon an 1996 Lonon Poocol

WhAt:

• 1972 intergovernmental treaty involving 86 countries.• Headquarters: International Maritime Organization in London, a UN organization.

• London Convention regulates pollution via dumping at sea (but not coastal runo).

• Some dumping pollution (such as scrap metal) is regulated, and some (such as mercury) is banned outright.

• 1996 London Protocol expands the London Convention to use the “Precautionary Principle” and reduce pollution.

• United States is party to Convention, but has signed but not ratied the London Protocol.

• US enforcement of London Convention by EPA under Marine Protection, Research, and Sanctuaries Act of 1972.

• Enforcement is by each country in its own waters and to ships sailing under its ag. No international enforcement.

hoW It ReLAteS to oIF: Bcas on laon acvs q aon o noanc aal n hNLC ons o wol

ocan, an nall ak plac n nnaonal was, Lonon Convnon s lvan. Ts lvanc as bn sbjc o

so scsson, owv, as Lonon Convnon las pn o sposal o was. Bcas OiF o cabon sqsaon wol

sqs cabon n p ocan, scsson o w OiF s o appopal pn o cabon as also bn as.


Jn 2007: Scnfc gop ss “San o Concn” o Lonon Convnon ov lascal ocan laon acvs.

Nov 2007: Lonon Convnon rsolon aops “San o Concn” an as a ocan laon alls n solon’s

pvw.

ma 2008: Scnfc gop oln wa ocan on laon nals an al so nknown sks.

Oc 2008: Lonon Convnon rsolon sas a no ocan laon acvs o an “la scnfc sac” o b fn

n 2009 sol b allow.

Fb 2009: tcncal Wokn gop as colocal sk assssn awok o OiF sac splan a sac s b

possvn. Ts pon os no l o cocal an o cabon cs o la sac.

Fb 2009: Lal Wokn gop poposs nw solons an nw bnn acls on OiF, olnn lao possbl s o

consaon o ll Convnon.

ma 2009: Scnfc gop n ro o cons pos o wokn ops an o sa olnn accpabl lvls o na

v nvonnal pacs o la scnfc sac .., xpns 200 x 200 k o sall.

FutuRe ReguLAtIon: Te London Convention is clearly grappling with the dicult issue of regulating scientic research at the suprana

onal lvl. A sa , s a cla ps owa scon o nonscnc OiF acvs. Spcfc poposals o Fba

2009 wokn ops an o o bans o all nonscnc OiF acvs o “sspnsons” o acv nl o aa can b a.

T qsons o cocalaon, colocal assssn, an o nocn/nns o laon av all bn as b non

o s solv. T Scnfc gop av sa o scss qsons abo ow c o an nvonnal pac o scnfc

sac s oo c an wll psn a po o ovnn bos o convnon wn n Lonon n all o 2009.

8/8/2019 22 3 Strong



biogeochemical modeling (Chu et al.,

2003; Rice, 2003). Meanwhile, Dan

Whaley, a ormer inormation tech-

nology entrepreneur, ounded Climos

Inc., a or-prot company setting out to

pursue the same goals as Planktos Inc.:

selling carbon credits rom ocean iron

ertilization (Riddell, 2008). Tus, by

2006, two companies operating in the

San Francisco Bay area—Climos and

Planktos—were developing the business

o iron ertilization.

In late 2006, it was reported that

Planktos donated carbon credits to two

Caliornia environmental organizations

to make them “carbon neutral” or 2007

(Industrial Environment, 2006), a claim

that was based on an upcoming pilot

demonstration o ocean ertilization.

At this time, Planktos was describing

itsel as an “ecorestoration” company,

seeking to replenish what was described

as diminished plankton stocks in the

ocean, in addition to sequestering carbon

or oset credits. In a 2007 presentation

to the US House Committee on Energy

Independence and Global Warming,

Planktos’ Russ George stated that “our

ocean plankton restoration pilot projects

will generate the rst substantial iron

seeded blooms aimed at serving our twin

purposes o restoring ocean plant ecosys-

tems and sequestering atmospheric CO2”

(George, 2007).

Plankos Fols Bo

i Can Fl

In early 2007, Planktos Inc. announced

plans to conduct a large ertilization

experiment in the equatorial Pacic near

the Galápagos Islands. Like the proposed

Markels-Barber demonstration, the

Box 2C. un Naons Convnon on Bolocal dvs CBd

WhAt:

• International treaty established at the Earth Summit in Rio de Janeiro in 1992.

• Dual purposes of biodiversity conservation and sustainable use and equitable distribution of resources.

• All UN nations are party, except the United States, which has signed but not ratied the treaty.

• Te Convention is administered by the UN Environment Programme (UNEP).

• Enforcement by individual ministries of member states.

hoW It ReLAteS to oIF: T Convnon las acons a an bovs, ncln an bovs. in s wa,

unknown ecological eects of large-scale OIF implementation fall under the purview of the Convention.


ma 2008 CBd dcson: “All lascal OiF acvs sol no b allow.”

• Makes exception for “small scale studies in coastal waters.” Coastal waters may be an aberration.

• Decision explicitly mentions commercial interests as a reason not to allow OIF.

• Decision passed because of ecological risks of OIF and uproar over Planktos’ experimental plans.• Widely viewed as a “UN moratorium” on commercial OIF activities.

FutuRe ReguLAtIonS: T CBd ss a OiF laon b on n coonaon w innaonal ma Oansaon

imO an Lonon Convnon. i calls o a lobal anspan conol an lao cans o b sabls, an s conslaon

w all pas nvolv o sabls a knowl bas abo assoca colocal sks.

note on CBd enFoRCement: in al 2009, gan sac ns c uN CBd COP 9 oao on ocan laon

n s cson o sspn inogan LOhAFeX OiF xpn. i an o nvonnal sk assssns an npnn

scnfc assssns o pojc, spcfcall nonn coasal wa splaon an cn colocal concns as b CBd.

Alo xpn was vnall vn n l, was a fs s o conspcfc nocn o nnaonal as on s

ss an as no Lonon Convnon wokn ops’ scssons on ow bs o la scnc o OiF.

8/8/2019 22 3 Strong



experiment was to be on a previously

unachieved scale o 10,000 km2; it would

be the rst pilot project in a planned

“Voyage o Recovery” (see Figure 5

or a sense o the relative size o this

experiment). Te company purchased aretired research vessel, Weatherbird II ,

rom the Bermuda Biological Station to

execute the experiment (Environmental

Protection Agency, 2007). Te scale and

seriousness o this proposal, coupled

with increasing concerns about risks to

marine ecosystems, mobilized environ-

mental NGOs. Te Canadian-based EC

Group called on the US Environmental

Protection Agency (EPA) to stop thePlanktos experiment (EC Group News

Release, 2007). Te World Wildlie

Fund argued that Planktos was taking

too big and too dangerous a leap with

the scale and intent o the experiment,

especially because it was near the

Galápagos Islands (Sullivan, 2007). Te

Sea Shepherd Society threatened to block

Planktos’ ertilization ship physically

(South Bay, 2007), arguing that it was a

violation o international laws on marine

dumping (the London Convention; Sea

Shepherd News, 2008).

With international law once again

in question, the legal arguments began

to mount. Te Scientic Group o the

London Convention issued a June 2007

statement o concern about Planktos’

plan (Scientic Group o the London

Convention Meeting Report, 2007). In

a statement submitted at that London

Convention meeting, the US EPA

announced that it would not permit

the Planktos plan to proceed under the

US Marine Protection Research and

Sanctuaries Act o 1972 (the US enorce-

ment o the London Convention) i

Planktos was ying a US ag rom

Weatherbird II (Parks, 2008; Scientic

Group o the London Convention

Meeting Report, 2007). Apparently,

Planktos assured the EPA that it would

not be sailing under a US-agged ship

(International Center or echnology

Assessment, 2007), which seemed to

contradict that Weatherbird II was a

US-registered vessel and would set out

rom a US port or the experiment.

Because o the proposed experiment’s

proximity to the Galápagos, the govern-

ment o Ecuador also issued statements

o alarm (Scientic Group o the London

Convention Meeting Report, 2007).

In the all o 2007, as Planktos’ vessel

prepared to leave the eastern coast o

the United States, the ull Conerence o

Parties to the London Convention issued

a statement o concern about the legality

and wise practice o large-scale ocean

iron ertilization activities, taking the

rst step toward explicit international

regulation o iron ertilization (London


Planktos’ experiment did not take

place (Courtland, 2008). Citing concerns

over disruption o their activities,

Weatherbird II le port headed to an

undisclosed location in the Atlantic

F 5. T lav ss o l pacs n ocan laon xpns, an n onsaons

ca o, o popos, b pva sco. A boo s an sa bas on ol o

zaav al., 2008 o s o pac a wol sl o ln hNLC ons o

Son Ocan.

8/8/2019 22 3 Strong



Ocean. When the ship approached the

Spanish-owned Canary Islands, report-

edly to pick up supplies, the Spanish

government reused it port entry

(Consumer Eroski, 2007), a decision

that Planktos blamed on environmental

organizations (Tompson, 2008). Te

ship eventually docked in the Portuguese

island o Madeira to take on needed

supplies (San Francisco Business imes,

2007). Investors pulled out o Planktos,

and, in early 2008, Planktos Corp. ended

its relationship with Planktos Inc., as

did Solar Energy Limited. Planktos Inc.

then suspended operations (Business

Wire, 2008; Kerry, 2008), citing both

a lack o unds and a “highly eective

disinormation campaign waged by

anti-oset crusaders” (Brown, 2008).

Several months later in June 2008, Russ

George started a new iron ertiliza-

tion “ecorestoration” company, named

Planktos-Science, though there has been

little activity other than Web posts rom

this company thus ar (see http://www.

planktos-science.com/).

Clos’ Pa Fowa

Tese events le Climos as the leading

company involved in the nascent

commercial iron ertilization business.

Since its inception, Climos made clear its

intention to conduct research in collabo-

ration with the scientic community,

and to this end brought in Margaret

Leinen, an accomplished oceanogra-

pher, and ormer Assistant Director or

Geosciences at the US National Science

Foundation, to be Chie Science Ofcer

(Climos About Us, 2008). Climos’ initial

plan was to attract substantial business

investment and to employ environ-

mental consulting rms to produce

codes o conduct or iron ertilization

experiments as a rst step toward

eventual verication or carbon credit

sale (Climos Press, 2007). Climos repre-

sentatives have attended international

meetings, UN meetings, and scientic

conerences to participate in debating

the uture o iron ertilization science.

At the same time, the company has also

made clear its plans to conduct its own

technology demonstration (Murray,

2008). In early 2008, Climos issued a

press release responding to Greenpeace

criticisms o plans or commercial OIF

(Allsopp et al., 2007). In particular,

Climos challenged what it described

as Greenpeace’s assumption that OIF

or carbon sequestration would require

large-scale and continuous ertilization,

something that “no commercial entity

has suggested should take place beore

a period o experimentation” (Leinen

et al., 2008). On its Web site and in the

press, Climos has announced plans or a

Southern Ocean demonstration experi-ment that would be “part o a new phase

o research ocused on the efcacy and

impact o moderately sized experiments

(< 200 x 200 km)” that would “emphasize

research related to export and sequestra-

tion as well as environmental impact”

(Climos FAQ, 2008). In a statement to

the press, Climos ofcials indicated that

they hope to conduct their rst trial by

the end o 2009 and to be able to startselling carbon credits shortly thereaer

(Murray, 2008). More recently, Leinen

has been identied as Chie Executive

Ofcer o the Climate Response Fund,

“a nonprot organization ormed to

provide unding and support or other

activities needed to explore innova-

tive solutions to the eects o climate

change” (Climate Response Fund, 2009).

At the time o this writing, it is unclear

whether the ormation o this new

nonprot organization will inuence

the plans o Climos.

rlao Cla is

On t hoon

In part due to the activities o Planktos,

Climos is operating in a vastly changed

regulatory arena than existed in the

early years o commercial interest in

ocean ertilization. Planktos’ proposed

experiment, and the vigorous response

to it rom environmental NGOs and the

London Convention regulators, showed

the rst signs o a negative eedback

loop. Up until this point, the trajec-

tory had been continued expansion

o commercial interest and proposed

the POteNt iNteLLeCtuAL reSOurCeS thAt

hAVe BeeN tied uP iN the OCeAN FertiLizAtiON

CONtrOVerSy yeAr AFter yeAr ShOuLd Be Freed

tO PurSue mOre eFFeCtiVe reSPONSeS tO the

PerVASiVe threAt OF CArBON diOXide emiSSiONS

ANd gLOBAL WArmiNg.

“

”

8/8/2019 22 3 Strong



demonstrations, despite the absence o

direct evidence or commercial claims

rom the results o scientic experi-

ments. Aer concerns were expressed at

the 2007 London Convention assembly

regarding the planned Planktos experi-ment in all 2007, representatives met

again in May 2008. Tey reiterated their

concerns about unchecked large-scale

ertilization activities, and dened

how iron ertilization t under the

jurisdiction o the London Convention

(Scientic Group o the London


Tat same month, members o the

UN Convention on Biological Diversity passed a decision on iron ertilization

(UN CBD, 2008), citing the London

Convention’s statements o concern.

Tey requested all member states to

ensure that ocean iron ertilization

activities do not take place, with the

exception o small-scale scientic studies

in coastal waters (see below), until there

is adequate scientic basis on which to

justiy these activities. Tey emphasized

that the excepted small-scale studies

could not be used or the generation o

carbon oset credits.

While the Convention on Biological

Diversity did not explicitly dene what

was meant by “small scale,” a report

submitted by the Intergovernmental

Oceanographic Commission (IOC), part

o UNESCO, to the London Convention

Scientic Group at Guayaquil in 2008,

proposed that OIF activities greater

than a size o 200 x 200 km (40,000 km2)

should be considered “large scale,” and

anything smaller would remain “small

scale” (Scientic Group o the London


Te area 200 x 200 km is two orders o

magnitude larger than the largest OIF

experiments to date (Figure 5).

Te stipulation o “coastal waters” in

the CBD statement was largely viewed

as an aberration, as most coastal waters

are not iron limited, and this is why

all previous scientic studies havetaken place in the open ocean (Owens,

2009; Alred Wegener Institute, 2009).

Nonetheless, because the stipulation

was written into the UN CBD language,

members o the LOHAFEX scientic

team ound themselves having to nd a

way to describe their open-ocean experi-

ment as “coastal” in order to proceed.

Tus, when providing their risk assess-

ment to the German Research Ministry during the experiment’s suspension (see

introduction above), they argued that

iron ertilization in the Southern Ocean

would stimulate the growth o “coastal

species” o phytoplankton, an argument

that was apparently accepted, as the

German ministry ultimately allowed the

experiment to proceed. I science and

policy are to move orward on this issue,

lines o communication between sectors

should be continually improved.

A ew months aer the Convention

on Biological Diversity decision, the ull

London Convention took up the issue o

ocean iron ertilization once more, and

passed a Resolution on the Regulation

o Ocean Fertilization, announcing that

all iron ertilization activities, with the

exception o “legitimate science,” were

in violation o the London Convention’s

regulations on marine dumping. Te

London Convention also decided that

technical and legal working groups

would meet in February 2009 to

determine what constitutes legitimate

scientic research, establish an assess-

ment ramework, and propose uture

regulations under the Convention. A

multi-step delineated environmental risk

assessment ramework was proposed

or uture experiments, including small-

scale scientic experiments (Report o

the First Meeting o the Intersessional

echnical Working Group on OceanFertilization, 2009). Te hope is to avoid

the kind o controversy and uncertainty

surrounding LOHAFEX by having a

system in place to prevent conusion

between scientic experiments and

geoengineering projects.

In May 2009, the Scientic Group o

the London Convention met to discuss

the report o the echnical Working

Group and attempt to urther dene theacceptable ecological impacts o “legiti-

mate scientic research.” Specically on

the agenda was a “Dra Action List or

Ocean Iron Fertilization,” proposed by

representatives rom Australia and New

Zealand, which lists upper and lower

limits or nutrient and chemical species

concentrations (dissolved oxygen, pH,

nitrous oxide, ammonium, and methane,

among others) altered in response to

a small-scale (less than 200 x 200-km)

scientic experiment. Dra Action Lists

are used by the London Convention

process to regulate substances on the

basis o their eects on the marine

environment; the 2009 version entitled

“Ocean Fertilization: Development o a

Dra Action List” is the rst step in the

process o answering the question, “How

much o a negative result rom OIF is too

much?” In the all o 2009, the governing

body o the London Convention will

take up the reports rom the meeting o

the Scientic Group.

What remains unclear is whether

these assessments o uture small-scale

scientic OIF experiments will be

conducted at the international level

8/8/2019 22 3 Strong



o the London Convention, or by the

science and research entities o the

individual countries involved. Future

regulation o larger-scale and nonscien-

tic OIF activities also remains unclear.

Te Legal Working Group o the LondonConvention proposed a set o possible

regulatory rameworks, ranging rom a

simply structured nonbinding resolu-

tion against large-scale OIF, to a ull

article amendment to the Convention

explicitly prohibiting it (Report o the

First Meeting o the Intersessional Legal

and Related Issues Working Group on

Ocean Fertilization, 2009). Te working

groups also avoided resolving the issue o whether commercialized carbon credits

could be sold as a product o “legitimate

scientic research,” leaving that question

to the ull Convention. What is now

clear is that the London Convention is

the central international legal rame-

work or this issue, and that regulation

o OIF will be a subject o continued

discussion and debate.

WhAt hAVe We LeAr Ned?

A rpa Ccl

Looking back, it is obvious that the

rst ew years o debate about the iron

hypothesis were a condensed version

o the 20 years to ollow. Small-scale

ocean ertilization experiments were

executed by oceanographers to address

specic scientic questions; ar-reaching

interpretations, conclusions, and rami-

cations were highlighted by the media

and by entrepreneurs, prompting a

response rom the scientic community

urging caution, ollowed by calls rom

academics and commercial-sector

proponents o OIF or more research.

Tis cycle has played out repeatedly as

the eld o ocean iron ertilization has

moved orward. And, despite the absence

o direct scientic evidence or OIF as

an eective long-term climate mitigation

tool, appeals or research on its efcacy

or this purpose have intensied over

the 20 years since the rst experiments,leading to larger and longer experiments.

Te dampening eedback rom negative

results, central to the advancement o

scientic research, seems largely absent

rom this cycle.

t Scnc dos No Sppo

OiF Fo global gonnn

Nearly two decades o scientic OIF

experiments have taught us that ironlimits productivity in several regions

o the ocean. We have learned that the

carbon export response to OIF is highly

variable—strongly regulated by the avail-

ability o light and silicate as inuenced

by physics, and also sensitive to the

interplay o many other actors that have

yet to be resolved. And we have learned

that on the temporal and spatial scales

o the experiments, carbon export is

oen quite small due to remineraliza-

tion o the phytoplankton bloom in the

surace waters. Models show that at the

limit—assuming complete macronu-

trient depletion and ertilization o the

Southern Ocean or 100 years—what

could be expected at most is global

sequestration o 1.0 Gt C yr-1 (able 2).

In all modeled scenarios, the amount

o CO2

sequestered is small relative to

the amount predicted to be released by

ossil uel burning, and the estimates

o sequestration have only gotten

smaller with more experimentation and

modeling (Denman, 2008). Furthermore,

models show that in order to maintain

the carbon sequestration, we would

have to continue to ertilize the entire

Southern Ocean with enough iron to

deplete macronutrients, in perpetuity.

Tis scenario is not realistic.

uncan an rsk

While the uncertainties about theefcacy o carbon sequestration rom

OIF as a geoengineering proposal

are high (Buesseler et al., 2008), the

certainty o ecological disruption is also

high. OIF or carbon sequestration is

designed to initiate a oristic shi to the

production o larger, bloom-orming

phytoplankton—in particular, diatoms

that are heavy and can sink rapidly. Tis

undamental alteration o the base o aood web would change the structure

and biogeochemical unction o the

community that depends upon it. Te

induced blooms would consume the

excess macronutrients at the surace

in HNLC regions, which, in combina-

tion with enrichment o deep waters

(e.g., Fuhrman and Capone, 1991),

would over time alter the biogeochem-

istry o the global ocean ecosystem.

Although we cannot predict the precise

changes that would occur, the only way

in which iron ertilization can work or

climate mitigation is to change deep

ocean chemistry and the way endemic

marine ood webs unction. Tere is

considerable risk in trusting inherently

uncertain predictions o such large-scale

and long-term alterations o the ocean.

Lont Ocan Cabon

Sqsaon o ion

Flaon is No Vabl

Fertilization-induced changes in

ecosystem unction would not only

have proound eects on the ecology o

huge marine ecosystems, but they would

also aect the potential efcacy o OIF

8/8/2019 22 3 Strong



as a carbon sequestration strategy. As

Gnanadesikan et al. (2003) point out,

in order to accurately model the net

global benet o carbon sequestration,

all downstream eects on biological

productivity must be counted, includingpotential disruption o sheries rom

the depletion o macronutrients in the

source waters o productive ecosystems.

Tese negative eects may outweigh

the benets o carbon export. Besides

the potential or changes in net global

productivity, OIF could stimulate

nitrous oxide production as a result o

increased remineralization o carbon

and nitrogen (Denman, 2008). Tiswould result in longer-term and ar-eld

changes in nitrous oxide production

that could potentially oset signicant

amounts o predicted green-house gas

benets o OIF (Law, 2008). It can thus

be argued that measurements associated

with individual experiments cannot

be adequate to veriy what would

ultimately be a long-term, large-scale

eect o many applications o iron

(Cullen and Boyd, 2008).

Tese complex downstream responses

to ocean ertilization make verica-

tion o net greenhouse gas reduction

through ertilization next to impossible

(Chisholm et al., 2001; Cullen and Boyd,

2008; Gnanadesikan and Marinov, 2008).

Furthermore, carbon export measured as

a result o a ertilization-induced bloom

would have to be reerenced to a baseline

rate o carbon export. As ocean ertiliza-

tion and carbon ux research has shown,

this natural rate o carbon export is

highly variable in space and time; estab-

lishing an appropriate baseline to grant

carbon credits or individual applications

would be exceedingly difcult, and rie

with uncertainty (Figure 6).

At present, there is no system under

the Kyoto Protocol’s Clean Development

Mechanism to provide or carbon

credits rom osets by marine carbon

sequestration (Powell, 2007–2008).

Tus, under the current internationalmechanism, any credits granted

would thereore have to be sold on

the currently unregulated “voluntary

carbon credit market.” Although Climos

Inc. submitted a carbon sequestration

methodology to Det Norske Veritas, an

international verication company, in

late 2007 (Climos Press, 2007), ofcial

approval or verication has not been

given to OIF as a carbon sequestrationmethodology. Nonetheless, in the uture,

international carbon credit regulatory

systems may well include provisions or

marine “sequestration” osets (Powell,

2007–2008). It will then be very impor-

tant or OIF proponents to show in their

plans that the eects o wide-scale, long-

term carbon sequestration rom OIFare predictable, acceptable, and statisti-

cally veriable across ocean basins over

decades. In our opinion, assessments o

individual applications are not enough.

Sol W Conn o ts OiF

o Cla maon?

Arguments have been made or 20 years

that OIF should not be pursued as a

“quick-x” or the climate problem. Wehope we have shown that the original

arguments have not been weakened

F 6. Cocal ocan laon, wc wol nvolv vala cabon cs,

wol av o onsa a onnc bloo wol no av ows

occ. Ts sall cloopll a a sows bloo nc b on aon

n LOhAFeX ccl. T o bloos a ccl n black. how wol on

pov a nnonall l was, l alon, wol no av bloo lk

nbon was? Image taken rom: http://www.awi.de/en/inrastructure/ships/polarstern/

weekly_reports/all_expeditions/ant_xxv/ant_xxv3/26_ebruary_2009/

8/8/2019 22 3 Strong



by new evidence over that interval.

Ocean ertilization will not solve the

CO2

problem, and i implemented or

prot, regardless o scale, has the poten-

tial to change the nature o the ocean

through the “tragedy o the commons”(Hardin, 1968). Perhaps it is time to

break the two-decade cycle o debate

and accept that we know enough about

ocean ertilization to say that it should

not be considered urther as a means

o climate mitigation. But our opinions

aside—and they are indeed opinions,

though science-based—a undamental

issue remains: the ecological and climate

mitigation response to OIF is scale-dependent (Buesseler et al., 2008; Cullen

and Boyd, 2008), and the biogeochemical

changes would be cumulative. Te only

way to test OIF as a climate mitigation

tool (i.e., to see i model projections

are right) would be to alter much o

the ocean system, perhaps irreversibly,

beore crucially important negative

eects could be evaluated with statistical

condence. We eel that the risk o doing

this does not compare well to even the

most optimistic predictions o potential

climate mitigation.

movn On

Climate change is already upon us.

Society needs to know what the ocean

will be like in a high CO2

world—which

ecosystems will be at risk as the ocean

warms and acidies, and how the altered

ocean will in turn inuence climate.

Understanding how ocean biogeochem-

ical cycles are linked, and the processes

that drive these cycles, is essential or

climate prediction. ransormational

developments in genomics along with

rapid advances in ocean observations and

modeling (Doney et al., 2004) allow us

to study the ocean as a system on scales

rom molecules to ocean basins, and we

are poised to ully integrate studies o

evolution and biogeochemistry (Woese

and Goldeneld, 2009). Tese develop-

ments open new vistas or understandingthe very basis o lie processes, and it is

these very lie processes that, scaled up,

regulate the concentration o CO2

and

other greenhouse gases in Earth’s atmo-

sphere. In this context, small-scale ocean

perturbation experiments are useul

tools or probing ecological and biogeo-

chemical relationships, and they should

continue to be used as such. Te potent

intellectual resources that have been tiedup in the ocean ertilization controversy

year aer year should be reed to pursue

more eective responses to the perva-

sive threat o carbon dioxide emissions

and global warming.

ACKNOWLedgmeNtS

ALS and SWC are supported in part

by unds rom the Gordon and Betty

Moore Foundation Marine Microbiology

Initiative, the US National Science

Foundation, and the US Department

o Energy. JJC is unded by the Natural

Sciences and Engineering Research

Council o Canada, the Killam rusts,

and the Ofce o Naval Research. None

o the authors have solicited or received

unds rom organizations or companies

or or against ocean ertilization. We

thank Jim Long or graphics, Edward

Boyle or his expert advice on one

part o the manuscript, Charles Miller

or extremely helpul comments and

discussion throughout, and E. Virginia

Armbrust, Heidi Sosik, Kenneth

Denman, and an anonymous reviewer

or their careul and insightul reviews

o the manuscript.

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