THE

BIOGEOCHEMISTRY
OF IRON

Philip Boyd
NIWA, New Zealand

OUTLINE
Why Iron?
Sources and sinks of iron
Fe recycling uptake and turnover
Fe biogeochemistry - examples from SOLAS
Climate change and Fe biogeochemistry
WHY IRON?

Behrenfeld et al. (1996)

Courtesy J. Cullen (WHOI 2007)
The Vostok ice core provided tantalising evidence
of the impact of changes in Fe supply on atmospheric
CO2 (Martin, 1990)

300

Fe (mol/kg ice)
[CO2] (ppmv)

280 1.5

260
CO2
240 1.0

220

200 0.5
Iron
180

20 40 60 80 100 120 140 160

Age (1000 yr)

Today
 IRON and CLIMATE
Marine biota play a key role in climate
by regulating atmospheric CO2 levels

One means of regulation is via the

BIOLOGICAL PUMP

The PUMP works most

efficiently when all of
the available nutrients
are utilised
 300
Links between iron and climate

Fe (mol/kg ice)
[CO2] (ppmv) 280 1.5

260
CO2
240 1.0

220

200 0.5
Iron
180

20 40 60 80 100 120 140 160

Age (1000 yr)

 Fe - SOURCES AND SINKS
Oceanic Inputs (1012 g / y)
10000
9000
8000
7000
6000
5000
Iron supply
4000
3000
2000
1000
0 Mackenzie et al.
Dust Rain
Mining Industrial Streamload (1979)
Most of the Streamload Fe is complexed by organic matter in suspended
sediment in estuarine and coastal environments forming Fe-rich sediments
 Predominant dust source regions and transport routes

Pye (1987)
Global aerosol iron flux
based on a sparse set of discrete samples (SEAREX, 1970s)
they miss the episodic nature of dust in many regions

Duce and Tindale (1991)

Boyle et al. 2005 Sedwick et al. 2005 Bergquist et al. 2006 Sarthou et al. 2007 Guieu et al. 2002

30N

30S

Jickells et al. 2005

Dust supply and profiles

Of dissolved iron
Courtesy S. Blain
Blain et al. subm. Bergquist et al. 2006
(U. Marseille)
Global aerosol distributions
Evidence of a dust storm from TOMS Aerosol
Index, April 22 -25 1998 NE Pacific
 Oceanic
supply of
iron - mainly
from upwelling
Trull et al. 2001

Morel & Price

2003

Trull et al. [2001]

Mesoscale jets supply iron to frontal regions

de Baar et al. (1995) - Polar Front (Atlantic sector)

Other iron supply mechanisms
Ice melt (Sedwick, DiTullio)
Offshore transport of Fe in eddies (Crawford, Whitney)
Coastal ocean - geomorphology (Bruland, Hutchins)

Upwelling - Cromwell undercurrent (Coale, Chavez)

Offshore
movement of
Haida eddies
(containing high iron
levels) in the
Gulf of Alaska

(images Gower,
NASA)
Iron transport from the Sea of
Okhotsk to the WSP Total Dissolvable-Fe conc. (nM)
Nishioka et al. (2007) 0 2 4 6 8 10
0

C2
50N C9 1000
C1
C3 C4
C4 C8 SEEDS
C1
2000
C3
C2

Dept (m)
C7
45N 3000 C5
C5 C7
KNOT C8
4000 C9
C0
C0
C10
5000 C10
140E 145E 150E 155E 160E 165E
KNOT
SEEDS
6000

Vertical profiles of Total dissolvable iron in the S Sea of

Okhotsk (Green), the Oyashio region (Red) and the WSP
(Blue)
 Iron in E. Antarctic Snow
(Edwards and Sedwick, GRL 2001)
mean solubility = 32% c.f dust solubility (1-10%)

# of 3
samples
% Fe sol
2

0
0 10 20 30 40 50 60 70 80
 SINKS FOR Fe

Fe distributions
provide clues
as to the main
sinks for iron

Surface depletion
is indicative of algal
uptake
From Morel and Price [2003]
Iron supplied is usually rapidly removed by
the marine biota

de Baar et al. (1995) - Polar Front (Atlantic sector)

iron-induced phytoplankton bloom
 Fragilariopsis kerguelensis
Iron uptake kinetics using natural
Antarctic seawater
0.4 Fragilariopsis kerguelensis

0.35
80 m
0.3

Km Fediss: 0.44 x 10-9 M

(d-1)

0.25
max: 0.31 . d-1
0.2

0.15

0.1
0 2 4 6 8 10

Fe dissolved (x10 -9 M )

Timmermans et al. [2004]

HIGH DIFFERENT PHYTOPLANKTON
GROUPS HAVE DIFFERENT
IRON REQUIREMENTS

?? LOW
Fe recycling

Biological acquisition and removal mechanisms

The picture that emerges is one of an extremely dynamic

trafficking in essential trace metals in sea water

Morel and Price [2003]

Fe chemistry is complex!!
photoreduction
PFe
Fe2O3
Fe(OH)3
colloids FeOOH
0
[FeCO ] 3
+ [Fe(OH) +2 ]
[FeOH ] [Fe 2+ ] [Fe3+]
[Fe(II)L]? ? ?
[Fe(OH) 2+]
Algal
Cell
sidero-

photoreduction ? ?
phores INTERACTIONS
WITH THE BIOTA
PHOTOCHEMISTRY [Fe(III)L]
organic complexes
(Courtesy of de Baar)
 Fe II and III - the redox cycle of Fe
oxidation
Fe(II) Fe(III)

reduction

The relative proportions of Fe(II) and Fe(III) in DFe in surface

seawater are dependent on the relative rates of reduction and
oxidation
In well-oxygenated seawater Fe(III) is the thermodynamically
stable form of iron
Fe(II) is relatively soluble in seawater, Fe(III) is less so
Fe(II) is primarily produced photochemically and biologically,
and is rapidly reoxidised to dissolved Fe(III)
Fe(III) may be converted to Fe(II) by reductive processes
Reductive processes include: photochemical, thermal (i.e by
organics), enzymatic, within microenviroments, formation of
Fe(II) organic complexes
 H
N NH2
O
NH
NH O
HO OH O O
A. OH
N
O H

Why is DFe so
NH HN
NH2 OH
HO NH
O HN O
H
O N
O
O
O
HO
HO

HN NH2

unreactive?
N HN
OH

B. O OH OH
OH O O O
H H H
N N N COOH
N N N
H H H
NH2 O O O
HO COCH HO COOH

O
C CH2
NH (CH2)2 N C CH3
CH2
OH O
C. HO C CO2H
OH O
CH2
NH (CH2)2 N C CH3
C CH2
O

More than 99.999% of dissolved iron in

seawater is organically bound (Rue and Bruland,
1995)
Fe(III) forms extremely strong organic complexes
Upon addition of 7 nmol L-1 Fe (III) to seawater, >
50% was complexed to a strong ligand within 2
minutes (Wu and Luther, 1995)
These organic complexes are referred to as iron-
binding ligands
 WHAT IS A LIGAND ?

Ligands are molecules

characterised by high
binding strength

The binding strength is measured electrochemically

and referred to as the
Conditional stability constant

So far two classes of iron-binding ligands

L1 or strong binding class [K FeL1, Fe(III)1 = 1013 L mol-1]
L2 or weaker ligand class [K FeL2, Fe(III)1 = 1011.5 L mol-1]

L1 are thought to be siderophores

L2 are particle breakdown products
 IRON ACQUISITION STRATEGIES
BY PHYTOPLANKTON

So far, only bacteria (heterotrophic & cyanobacteria have

been shown to produce siderophores

So how do eukaryotic phytoplankton (e.g. diatoms) acquire

iron required for photosynthesis, respiration.?

Hutchins et al. (1999) reported that eukaryotes could use

other chelated iron species (Fe bound to porphyrin structures)

Therefore competition of different chelated iron spps may exist

Diatoms can reduce Fe(III) extracellularly through enzymatic

processes and membrane transporters
Spinning theFERROUS WHEEL
(Kirchman, 1997)
 0.5 pM/d

(54%) (30%) (10%) (6%)

Detrital Fe Lithogenic Fe Dissolved Fe Biogenic Fe

300 pM 165 pM 55 pM 3.0

Producer
2.5 (?) 22 pM
s
(0.14/d)
3.0
Heterotrophic
4.4 11 pM Protozoa
(0.1/d)
1.1

0.6 Heterotrophic
4.6 pM Metazoa
(0.05/d)
NE Pacific 50N 145W
Total Fe 560 pM
Biogenic Fe 38 pM
80 m

0.5 pM/d
Pelagic Fe budgets point to rapid
recycling by the biota (Morel and Price, 1998)
SOLAS Science Plan
Activity 1.4 Iron and Marine Productivity

MESOSCALE IRON ENRICHMENTS

Boyd et al. (2007)

 Iron is added to
the ocean along with
the tracer SF6

An initial area of 4.00

70 km2 is enriched
2.00

with Iron The formation of

-144.83 -144.80
Long
-144.77 -144.74 -144.71 A coherent 0.00

50.22 C68

50.2
patch of high -2.00 C67

50.18
SF6 is used to
-4.00

track the
Lat

50.16 C69

50.14
enriched waters -6.00

50.12 for weeks -8.00

50.1 -4.00 -2.00 0.00 2.00

 The resulting blooms are large
enough to be viewed from space

The bloom as it develops

provides a laboratory to study
concurrent changes in physical,
chemical and biological signals
including climate-reactive gases
DIFFERENT MICROBES
DOMINATE EACH PHASE OF
THE BLOOM
500 160
140
400
120
mmol m-2

POC 300 100

Y Axis 2
80
200 60
40
100
20

0 0
10 15 20 25 30 35
SERIES Days
Blooms and gas production /consumption
Different groups influence gas concentrations in seawater

Comparison of radiative forcing IPCC (1996)

3

Global mean radiative forcing /W m-2

Halocarbon
N 2O
2
CH4

INDIRECT GREENHOUSE
1
DIRECT TROPOSPHERIC AEROSOL
CO2
CCN

-1

-2
Direct Greenhouse Tropospheric ozone Fossil fuel soot Indirect tropospheric (CCN)
Stratospheric ozone Sulfate Biomass burning Solar
 CO2 and bloom development

Phytoplankton fix carbon

A small but significant

proportion of this C
settles out of the surface
ocean

To restore equilibrium
CO2 is drawn down into
the ocean
 25 fCO2
Temporal development of C 20
(D18)
350

fixation in relation to the phases 15

340

330

of a bloom 10 320

310
5

4e+5 0
300

290

-5 280
Diatoms (cell L-1)
270
-10

3e+5 -40 -35 -30 -25 -20 -15 -10 -5 0 5

2e+5

1e+5

0
10 15 20 25 30 35
Days
BLOOM DECLINE
CAN TAKE PLACE
Bloom
VERY RAPIDLY
day 19

Bloom on
day 24

Boyd et al.
[2004]

Chlorophyll (mg m-3)

Exploring Fe
Biogeochemistry in
HNLC waters using
an inert tracer SF6

FeCycle

Boyd et al. [2005]

Croot et al.
(2007)
 15 1
Aeolian 0.

?? 10 0.

0.

5 0.

Mixed layer 0.

0 0.

0.

-5 0.

0.

-10 0
-10 -5 0 5 10 15
Kilometers

Lateral
advection Biological
recycling

Vertical
PFe Export
Diffusivity Biogenic Vs.
Lithogenic Fe export

Fluxes measured during FeCycle

 Fe uptake (nmol l-1 d-1)
0.00 0.05 0.10 0.15 0.20 0.00 0.05 0.10 0.15 0.20
0 0
A B
10 10

Depth (m)
20 20

30 30
total
> 20 m
40 5-20 m 40
2-5 m
0.2 - 2 m

50 50

0.00 0.05 0.10 0.15 0.20

0.00 0.05 0.10 0.15 0.20 0
0
C D
10
10

20
20

30
30

40
40

McKay et al. 50 50

(2005)
 How fast is the FERROUS WHEEL spinning?

Particulate Fe Pool 500

#
Phytoplankton Euky 2.4, Auto flag
7.8

Bacterioplankton Sync 67.1 Het bact 28.4

Grazers

Ciliates 6.2 Het flag 2.8

Viruses Grazers Bacterioplankton

Detritus
0.9-
70 Inorganic Fe 1.4 Phytoplankton
Herb
16.5-18.4
Sync 22.2-84.6
Bact Fe-L complexes Eukary 0.81-2.54
15.0-25.5
Auto flag 1.8-9.9

Dissolved Fe Pool

Pools are pmol Fe L-1,

and rates as pmol Fe L-1 d-1. Strzepek et al. (2005)
 15 1
Aeolian 0.

?? 10 0.

0.

5 0.

Mixed layer 0.

0 0.

0.

-5 0.

0.

-10 0
-10 -5 0 5 10 15
Kilometers

Lateral
advection Biological
recycling

Vertical
PFe Export
Diffusivity Biogenic Vs.
Lithogenic Fe export

Fluxes measured during FeCycle

Vertical & lateral iron supply terms from SF6

2.7

2.4
-20
2.1

1.8

-40 1.5

1.2

-60 0.9

0.6

0.3
20 40 60 80 100 120 140 160 180 200 220 240
-0.3

hours Log SF6

Boyd et al. (2005)

Iron IN and iron OUT

Frew et al. (2006)

 Aeolian
500 (a)

Mixed layer
5 to 50 DFe (b) [9 mol m-2]
450 to 495 PFe (c) [34 mol m-2]

2453 to 4055 (e)

Lateral
advection Biological
recycling
0 (d) >1976 (f)

Vertical
PFe Export (h)
Diffusivity (g)
216+27 to 548+128 Biogenic Fe export (i)
15+3
139+31 to 352+123
Lithogenic
Boyd et al. (2005) 77+7 to 196+9
 Iron biogeochemistry
and climate
Land and ocean impacts

Levitus (1999); Keeling & Whorf

How will climate change alter dust supply to the ocean?
IS MONITORING ENOUGH?
Modelling dust deposition rates will
be an essential tool

Mahowald et al.,JGR 104,15895-15916 (1999)

(g m-2 yr-1) N. Mahowald et al. (1999)
Factors influencing dust
deposition / Fe supply
E
C, D

A, B F,G

A Aridity, Soil Moisture

B Human Activity, Dust Size Spectra
C Dust Transport Routes
D Dust load - Carrying Capacity
Solubility
E Wet or Dry Deposition (solubility)
F Algal Community (Fe-deplete ?)
G Fe requirements (Diatoms, N-Fixers)
HOW WILL THE OCEAN
IMPACT IRON SUPPLY?

COAM simulations
for 2070 MINUS present
day

Boyd and Doney, 2002

 IRON BIOGEOCHEMISTRY
Conclusions

Iron Biogeochemistry is a rapidly emerging

Field (SOLAS; GEOTRACES)
Adding iron to the oceans continues to attract
commercial interest and remains controversial
The impact of climate change on iron supply
has many unknowns
New approaches such as iron isotopes hold great
promise
Dust flux overlaid on the NO3 distribution (M)
in the upper ocean
NOAA world ocean atlas, 1994

Atmospheric Fe flux
(mg m-2 yr-1)
10
Duce et al. 1991
100
1000
1000
100

100 10 1

10
SOLAS Science Plan

FOCUS 1

Activity 1.4 Iron and Marine Productivity

Natural and anthropogenic changes in climate and global

biogeochemistry will alter the atmospheric input of aerosols
containing iron and other trace metals to the ocean which may
cause changes in planktonic production and foodweb structure,
resulting in altered carbon partitioning and biogenic
air-sea gas fluxes
Boyle et al. 2005 Sedwick et al. 2005 Bergquist et al. 2006 Sarthou et al. 2007 Guieu et al. 2002

30N

30S

OLIGOTROPHIC GYRES
Courtesy S. Blain
(U. Marseille)

Blain et al. subm. Bergquist et al. 200

Labile iron in eddies
decreases steadily in
concentration from high
values in coastal and slope
regions. But even after 12
months, it is not down to
background levels below
the mixed layer.

24.0

24.5

25.0

25.5
Sigma-Theta

26.0 Plotted at left are labile

iron levels determined
26.5
by Keith Johnson of
27.0
IOS/DFO, as posted on
the DFO Haida Eddy
39 NE Gulf of Alaska 02/2001 49 Haida-2001 0 months
27.5 Web site.
53 Haida-2001 0 months Haida-2000 4 months
Haida-2000 8 months 44 Haida-2000 12 months
28.0 Labile = unfiltered, pH 3.2
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 for 1-2 h.
Labile iron, not filtered (nM FeIII)
 Offshore gradients in DFe in the
NE subarctic Pacific (nmol L-1)
0.7
0.6
Fe distributions
0.5
provide clues 0.4
as to the main 0.3

sinks for iron 0.2

0.1
0
coastal shelf offshore P20 P26
Boyd et al.
Indicative of rapid and effective removal in the Unpubl data
coastal ocean
However, in many regions a few episodic
dust storms may supply most of the
annual dust flux

So how do we monitor dust events?

fe ratio = new Fe / (new + regen Fe)

ef ratio = exported Fe / (new + regen

Fe)

Boyd et al. (2005)

SOLAS Science Plan

FOCUS 1

Activity 1.4 Iron and Marine Productivity

The Future climate change and Fe

biogeochemistry
SOLAS Science Plan

FOCUS 1

Activity 1.4 Iron and Marine Productivity

Natural and anthropogenic changes in climate and global

biogeochemistry will alter the atmospheric input of aerosols
containing iron and other trace metals to the ocean which may
cause changes in planktonic production and foodweb structure,
resulting in altered carbon partitioning and biogenic
air-sea gas fluxes
 DFe (nM)
0.00 0.05 0.10 0.15 0.20 0.25 0.30
0

50

100

150
(Measures & Vink, 2001)
200 Dissolved Fe profiles:
Spring 61S
Summer 61S little decrease in DFe during
250
the growth season

Indicative of a key role

for the recycling of Iron
 Observed Ocean Iron Distribution: Surface

Compilation in Parekh, Follows, Boyle, GBC, (2005)

 H
N NH2
O
NH
NH O
HO OH O O
A. OH
N
O H
NH HN
NH2
OH
HO NH

Forms of Iron
O HN O
H
O N
O
O
O
HO
HO

HN NH2

H
N HN
OH

B. O OH OH
OH O O O

in Seawater
H H H
N N N COOH
N N N
H H H
NH2 O O O
HO COCH HO COOH

O
C CH2
NH (CH2)2 N C CH3
CH2
OH O
C. HO C CO2H
OH O
CH2
NH (CH2)2 N C CH3
C CH2
O

Dissolved Colloidal Particulate

Dissolved two oxidation states - Fe(II) and Fe(III)

Mainly present in non-reactive forms in the upper ocean

Colloidal poorly understood

Particulate biogenic, lithogenic, detrital

Lithogenic iron present as oxyhydroxides, silicates and
aluminosilicates
Fe silicates and aluminosilicates are mainly very unreactive
- contribute little to dissolved Fe in seawater and their fate
is governed by coagulation and settling processes
 Who produces Ligands?

Field techniques at present are insufficiently sensitive to resolve

the nature of iron-binding ligands

Microbial studies on soil have revealed that terrestrial fungi and

bacteria can produce SIDEROPHORES high affinity Fe(III)
chelators which form the basis of iron-transport systems.

Microbes release siderophores into their external environment,

which chelate and solubilise iron present in minerals, adsorbed
onto particle surfaces or bound within existing complexes

Lab studies show that marine bacteria also produce siderophores with similar
conditional stability constants as L1 class ligands in the surface ocean
 Marine viruses also play a key role in Fe recycling

Aeolian Input Fe 2+
Inorganic
forms
Grazing
Fe 3+

Fe (2+) complexes Fe (3+) complexes

(cell products/ligands) (siderophores)

160 - 181
Viral pM d-1
20 - 31 lysis
pM d-1
20 - 80
pM d-1
Eukaryotes Prokaryotes

export

Poorvin et al. (2005)

 THE FOODWEB AND IRON SUPPLY

Grazing leads to
release of Fe in more soluble forms due to low pH in the gut

(Barbeau et al. 1996, 1998)

SOLAS Science Plan

FOCUS 1

Activity 1.4 Iron and Marine Productivity

Examples from SOLAS

SERIES C-SOLAS Fe and biogenic gases

FeCycle NZ-SOLAS Fe biogeochemistry
Observed Ocean Iron Distribution: 1000m
 FEW MESOSCALE IRON-MEDIATED BLOOMS
HAVE REACHED THEIR END-GAME

Boyd [2004]
Indirect evidence of aerosol Fe
Inputs near the FeCycle site
Boyd et al. (2005)
 mmol m-3 DFe (nmol L-1)
0 2 4 6 8 10 12 14 16 18
0.00 0.02 0.04 0.06 0.08 0.10
0
0
NO3

20 20

Depth (m)
40 40

60
60

McKay et al. (2005)

a) b) c) d) 300

Fe (mol/kg ice)
[CO2] (ppmv)
280 1.5

260
CO2
240 1.0

220

200 0.5
Iron
180

20 40 60 80 100 120 140 160

Age (1000 yr)

Fe*>0 Fe*< or =0 Fe*<<0 Fe*<0

pulsed sustained episodic episodic
sustained
days weeks weeks centuries
10 km 100 km 1000s km 1000s km

Boyd et al. Fig. 2

Air mass back
Trajectories from
The FeCycle site