Presentation by Jonathan Cole

1. Global C cycle with role of Inland Waters
This is a presentation that combines work from Cole’s ECI Book: Cole, J.J. 2013.
Freshwater ecosystems and the carbon cycle. In: Kinne O (ed) Excellence in ecology.
Book 18. International Ecology Institute, Oldendorf/Luhe 146 pp) and from his chapter
in a recent text book on ecosystem ecology (Cole, J.J. 2012. The Carbon Cycle.
Chapter 6, pp 109-136 IN: Weathers, K, D. L. Strayer, and G.E. Likens (eds).
Fundamentals of Ecosystem Science. Elsevier, New York. 312 pp.
• Both books are available for sale by the publishers.
• Cole (2012 at: http://www.int-res.com/book-series/excellence-in-ecology-
books/ee18/
• And Weathers et al. (2012) at: http://store.elsevier.com/Fundamentals-of-Ecosystem-
Science/Kathleen-Weathers/isbn-9780120887743/
• Partial support for Cole in both cases came from the National Science Foundation,
(Cole, J.J. OPUS: Terrestrial carbon in Aquatic Ecosystems: A synthesis. NSF-DEB
1256119. 15 February 2013-14 February 2016) and from the Cary Institute of
Ecosystem Studies. An earlier version of this talk was presented at a meeting of the
Association for the Sciences of Limnology and Oceanography (ASLO), Cole, J. J.;
“Terrestrial support of lake food webs: a weight of evidence argument.” (Abstract ID:
13330). Joint Aquatic Science Meeting. Portland Oregon, May, 2014.
• •This presentation may be helpful in teaching about the global C cycle in general and
the role of inland waters in that cycle.

2. Outline
• Ecosystem boundaries at the global scale.
• What is a “global” biogeochemical cycle?
• Major pools of C on earth
• C cycle at several time scales:
– Modern (perturbed)
– Pre anthropocene (past 10,000 years)
– Glacial- interglacial scale (400,000 years)
– BREAK
– Earth’s history
• Basics of the C cycle and its links to O
• A counterintuitive idea about atmospheric O2?
• The regulation of a global cycle depends on the
time frame considered.

3. An ecosystem is defined as a spatially
explicit unit of the Earth that includes
all of the organisms, along with all
components of the abiotic
environment within its boundaries
– Likens 1992

4. When looking at
the Earth as an
ecosystem, most
scientists draw
boundaries between
the “solid” planet
and the
atmosphere. Use
inputs and outputs
from the Earth to
atmosphere as
ecosystem fluxes.

5. Marine Sediments 20,000,000
At least 9,000,000 is organic C
Land
450 plants
700 detritus
Ocean
5 plants
3000 DOC
38,000 HCO3
Atmosphere 760
102/y 98/y100/y 100/y
Terrestrial soil - 2150;
Lake sediments - >25,000

6. Reservoir C mass (Pg) comments Reference
Earth 100,000,000 Poorly known Schlesinger (1997)
Sedimentary
rocks - carbonate
65,000,000 Schlesinger (1997)
Sedimenrary
rocks- carbonate
16,000,000 Schlesinger (1997)
Marine dissolved
carbonates (DIC)
38,000 Sum of dissolved
CO2, HCO3 and
CO3.
Sundquist and
Viser (2005)
Large lake
sediments
19,510 Most in African
rift lakes
Alin and Johnson
(2007)
Fossil fuel (coal,
oil, natural gas)
5,200 Known plus likely
reserves
Sundquist and
Viser (2005)
Terrestrial soils 2,150 Sundquist and
Viser (2005)
Atmospheric CO2 750 Modern,
industrial, rising
Houghton (2005)
Reactive marine
organic C
650 Sundquist and
Viser (2005)
Terrestrial
vegetation
560 Houghton (2005)
Marine biota 2 Houghton (2005)

7. Modern- perturbed C cycle

11. The modern global C balance
• Atmospheric CO2 has risen more rapidly in the
past century than at any other time in earth’s
history.
• Why is atmospheric CO2 rising?
• What is the evidence for the causes?
• How strong is this evidence?

12. Suess Effect
Change in 14C (and 13C) in the
atmosphere due to human process.
Named for Hans E. Suess
What changes and why?
Evidence Item #1

13. Decline in 13C of CO2

14. Decline in atmospheric 14C
coincides with industrialization.
What happens to this record
after 1950?

15. From (Levin et al., 2010).

16. World Climate Report
Evidence Item # 2. Atmospheric CO2 is highly correlated to the
global human population. R2> 0.95

17. CO2 versus fossil fuel use- global
Fossil fuel use - millions of metric tons per year
0 2000 4000 6000 8000 10000
CO2MaunaLoa(ppmv)
260
280
300
320
340
360
380
400
year 1800, extrapolated from other data
Y = 0.013X + 275; r2
= 0.97

18. Saga Commodities INC
Percent of global CO2 emissions by “country”

19. Saga Commodities INC
MetrictonsCO2percapitaperyear

20. Global C balance in Gt y-1
rough numbers after Schimel et al. 2001
• Emissions to atmosphere 6.5
• Increase in atmosphere 3.1
• Oceanic gas exchange -1.5 (physical)
• Net “terrestrial sink” -1.9 (biological)
• How are these numbers validated?

21. Modern atmospheric CO2
• Rising rapidly
• Fossil fuels as cause of increase supported by:
mass balance
isotopic evidence (14C and 13C)
correlation to human population growth
correlation to global fossil fuel use
lack of other credible explanations
What is the story for the pre-industrial period and
earlier time frames?

22. Past 1500
years

23. Past
160,000
years

24. Years before present
-400000 -300000 -200000 -100000 0
180
220
260
300
340
1000 1200 1400 1600 1800 2000
AtmosphericpCO2(atm)
240
280
320
360
Calendar year
1950 1960 1970 1980 1990 2000 2010 2020
300
320
340
360
380
400
C
B
A
Very long –
400,000,000
years
Past 1000 y
Recent
record
CO2 in the
distant past
has been
nearly as
high a
present- the
rate of
increase at
present is
unique

25. Past 10,000 years of atmospheric CO2
• Relatively stable.
• Not decreasing. (Falkowski and Raven)
• If organic C was stored on land, where did CO2
come from?
• What C supported terrestrial export production
which is near 0.5 Gt C y-1
• Volcanism -not larger than ~0.09 Gt y-1

26. Atmosphere
Increasing rapidly
3.1 Gt y-1
Ocean
sediment – 0.12 Gt y-1
Modern (50 y)
1.3Gt y-1
~1.9 Gt y-1
Terrestrial NEP > 1
Gt y-1
6.3 Gt y-1
Volcanoes
<0.09 Gt y-1

27. Atmosphere
Increasing slowly
0.02 Gt y-1
Ocean
ocean sediment buries
0.12 Gt y-1
Post glacial (10,000 y)Volcanoes
<0.09 Gt y-1
??Gt y-1
Values after
Sundquist 1993
Export >
0.4 Gt y-1

28. Pre-anthropocene balance sheet
in Pg C for past 10,000 years or so
• Inputs to atmosphere:
– Volcanism 0.09
– Change in atmospheric standing stock of CO2 < 0
• Outputs from the atmosphere
– Burial of organic C in marine sediment 0.12
– Terrestrial NEP
• Increase in plant biomass ~0
• Increase in soils and sediments 0.06
• Export of POC and DOC in rivers 0.4
– Sum of Outputs 0.58
• Missing source to atmosphere = 0.58 – 0.09 = 0.49

29. Where did the missing atmospheric source come
from?
• Need 0.49 Pg C y-1
• Did not come from land
• Did not come from volcanism
• What is left?
• Area of global ocean 361 X 106 km2
• That is 361 X 1012 m2;
• 0.49 Pg C= 0.49 X 1015 g C
• Or an imbalance of 1.4 g C m-2 y-1
• Easily possible for an excess of R over GPP in the ocean

30. Can we account for that 0.49 Pg y-1 imbalance in
the ocean
• Several steps to get there:
• Review the algebra of GPP, R and NEP
• Rewrite these as a mass balance equation
• Apply this to the ocean

31. Components of Productivity
CO2
GPP
NPP
Detritus and
exudates
Not
decomposedExported
Buried (Sediments
and SOM)
Consumers
Ra
Decomposers
Rh
Plant biomass
accumulation
NEP
(Rt = Ra + Rh)

32. GPP review
• GPP = total photosynthesis (> 0)
• R = total respiration (> 0)
• NEP =GPP-R (may be + or -)
• When NEP is +, equals burial plus export
• When NEP is -, net heterotrophy

33. NEP algebra.
• External Import from Outside ( Ie)
• Export from ecosystem (E)
• Burial (export to sediments) (B)
• GPP (gross primary production)
• R (total respiration in the system)
• Total Inputs = GPP + Ie
• Total losses = R+E+B
• Total Inputs = Total Losses (conservation of
matter)

34. NEP Algebra Continued
• Since NEP = GPP-R, we can rearrange
• (GPP-R) = E+B-Ie or:
• NEP = E + B – Ie
• So you do not need to measure GPP or R to
get NEP.
• If Ie is > (E+B), NEP is NEGATIVE

35. Terrestrial
Biosphere
500 -1000 Gt
Terrestrial
detritus
1000-2000 Gt
Marine
Biosphere
2 - 4 Gt
Marine
detritus
500 -1000 Gt
Marine
sediments,
organic
20,000,000 Gt
Atmosphere 760 Gt
~48 Gt/y photosynthesis~52 Gt/y photosynthesis
Biological parts of the C cycle (after
Holland, 1993).
-2 -1y
0.12 Gt/y0.4 Gt/y
river
transport
whole ocean net heterotrophy is
Burial + Export - Import
0.12 –0.4 = -0.28 Gt/Y or
OR ~0.8 g C m
burial
R ~100-0.12
99.8Gt/y

36. Let’s make the equation clearer
• Import from land via rivers = 0.4 Gt C/y
• Export from the ocean = ~0
• Burial in marine sediments = 0.12
• NEP = E + B – Ie
• NEP = 0 + 0.12 -0.4 = -0.28 Gt C/y
• This is about 0.8 g C m-2y-1

37. Correct order of magnitude
• Needed 0.49 Pg C y-1 ( 1.4 g C m-2y-1)
• Calculated that R >GPP by 0.21 Pg C y-1 or about
0.8 g C m-2y-1
• We are very close and easily within error limits.
• Other sources of marine CO2 to the atmosphere:
– Coral reef building
– Precipitation of calcite and aragonite shells
– HOMEWORK- explain how coral reefs, shells and the
manufacture of concrete are all CO2 sources

38. Are you disturbed?
• The modern ocean is presently a sink for atmospheric
CO2 of about 2 Pg C y-1
• Using modern values, we calculate that R exceeds GPP
by about 0.3 Pg C y-1
• Why is the modern ocean NOT a source of CO2 to the
atmosphere?
• Because atmospheric CO2 is rising! The ocean is a slight
source of CO2 to the ocean but it is trapped.

39. Outline
• Ecosystem boundaries at the global scale.
• What is a “global” biogeochemical cycle?
• C cycle at several time scales:
– Modern (perturbed)
– Pre anthropocene
– Glacial- interglacial scale (400,000 years)
– BREAK
– Earth’s history
• Basics of the C cycle and its links to O
• A counterintuitive idea about atmospheric O2
• What role to freshwater systems play in the global C
balance?
• The regulation of a global cycle depends on the
time frame considered.

40. Back to global – let’s link C and O
cycles over earth’s history

41. 0.00
0.05
0.10
0.15
0.20
0.25
1 2 3 4
Billions of years before present
pO2(atm)
cyanobacteria
eucaryotes
Land plants
mammals

42. Where does oxygen come from?
• Photosynthesis
• Balance between GPP and R
• GPP-R=NEP= org C burial.
• Atmospheric Oxygen comes from org C burial.
• If atmospheric O2 has been “flat” for the past
500,000 years, what does that imply?

43. What ever controls organic C burial
controls atmospheric O2
• O2 >> 0.2 atm leads to increased fire.
• O2 << 0.2 atm unsuitable for most aerobes
• What controls C burial?
– Mayer hypothesis
– Oxygen hypothesis. (Harnett et al)

44. Mayer 1994
0
5
10
15
20
25
0 10 20 30 40
Surface area (m2/g)
OC(mg/g)
Clay rules!
Where does clay come from?

46. Foree and McCarty 1970 and many
others
0
25
50
75
100
0 100 200 300
time (days)
percent
remaining
aerobic
anaerobic

47. Betts and Holand 1992
0
40
80
120
160
0 100 200 300
Bottom water O2 (uM)
Burialefficiency%

48. Hartnett et al, Nature 1998
• What is the debate they bring up?
• What is the new twist here.
• What is the “experiment”

49. Oxygen exposure time (yr)
0.01 0.1 1 10 100 1000
10
20
30
40
Hartnet et al.

50. Hartnett et al, Nature

51. GAIA (Lovelock, 1991)
• Hypothesis: Earth is kept in a state favorable
to living organisms by (in part) living
organisms.
• Theory: sees Earth as system in which
evolution of organisms is tightly coupled to
evolution of the environment. Self regulation
of climate and chemistry are emergent
properties of this system

52. Thank you.
• I am willing to meet with you by skype when
you have time, if you want to.

53. Organic C burial in lakes is large
• Natural lake organic C burial
– 0.065 Gt y-1 (Mullholland and Elwood 1982)
– 0.034 Gt y-1 (Dean and Gorham 1998;
Stallard 1998)
• Lakes sequester 28 to 54% as much organic
C as does the global ocean!
• Oceanic organic C burial ~0.12 Gt y-1
• See Cole et al. 2007, Ecosystems

54. data of Dean and Gorham (1998). Units
are Tg y
-1
organic C. Total is 420 Tg y
-1
or
0.42 X 10
15
g C y
-1
Note Ocean may be as
low as 60 and Reservoirs >200.
Ocean basin
(130)
Reservoirs (160)
Small Lakes (23)
Large Lakes (6)
Inland Seas (5)
Peat lands
(96)

55. Why do lakes bury so much organic C?
• Rich theory of C preservation in the sea
– Oxygen exposure time hypothesis
– Sorptive preservation hypothesis
• Poorly developed theory in freshwaters.
– Low oxygen (a real possibility)
– Low sulfate (especially compared to ocean)
– High lignin (plus low O2) – can be dismissed
• Certainly not close to a universal law of C
burial in freshwaters.

56. High organic C
content in
freshwater
sediments.
This Danish
man from 500
BC (so
somewhat older
than our St.
James) was
preserved in bog
sediment.

57. Dr. Morten Sondergaard a
living Dane and scientist.

58. Why did Morten’s progenitor preserve
– or why do freshwater sediment have
so much organic C?
• (From the Tollund man web site)
• No oxygen, therefore no bacteria, and no
rotting.
• Sphagnum inhibits bacteria
• Special acids inhibit bacteria
• Tannins ‘tan’ the hide.

59. Burial Efficiency- Oxygen exposure time
Hartnett et al. 1998 Nature
Burial Efficiency = Burial / Input = Burial / (Burial + Respiration)
Oxygen exposure time (yr)
OrganicCBurialEfficiency(%)

60. An empirical organic content model
Hakanson 2003
IG = loss on ignition (%DW)
SMTH= 52 week smoothing function
ADA = drainage area; A lake area
Drel = relative depth;
color = water color
Drel is the relative depth (= Dmax · √π/(20 ·
√Area),

61. Predicted = 0.9024* Observed + 2.4492
R
2
= 0.8189
-20
0
20
40
60
0 20 40 60
Observed IG
PredictedIG
NOTE – oxygen is NOT part of this model!!

62. Whole-lake areation experiment
Engstrom and Wright 2003
• 10 lakes in Minnesota
• Cores taken before and after aerating 5
• 5 lakes as ‘control’
• Areation was from 8 to 18 Years. Near
continous.
• Irregular effect of aeration on total sed
accumulation
• Areated lakes did not decrease in organic
content.

63. Engstrom and Wright 2003
Aerated
Non- Aerated

64. Carbon in freshwaters – summary so far
• Globally, lakes bury about 40% as much organic C as
does the ocean.
• We do not have good models for C preservation in
lake sediments. Research opportunity.
• River delivery of organic and inorganic C to the ocean
is an important term in the global C balance.
• Lakes and rivers tend to be net heterotrophic – must
respire some terrestrial C.
• Does this terrestrial C move up the food web?
Research opportunity.

65. GPP R
sedimentation
Net gas flux
transport
Do Freshwater systems matter in the global C balance?

66. NCEAS working group
Cole et al. Ecosystems
2007
Integrating Terrestrial and
Aquatic C Cycles (ITAC)
Rob Streigl, Nina Caraco,
Lars Tranvik, Bill
McDowell, Carlos Duarte,
Jack Middleburg, John
Melack, Yves Prairie,
Pirkko Kortalainen, John
Downing, Jon Cole

67. Rivers also transport “atmospheric” C
• Terrestrial OC in rivers to the ocean (units are Gt y-1
(from Meybeck 87; Sarmiento and Sundquist 92;
Stallard 98:
• Dissolved organic C - 0.23
• Particulate organic C - 0.30
• Total organic transport 0.53
• Note implied loss from land is larger by 0.23 number
or ~ 0.75 Gt y-1 to balance riverine gas flux.

68. Dissolved inorganic C (DIC)
• DIC is CO2 +H2CO3 + HCO3 +CO3
• DIC in rivers is dominated by HCO3
• At pH 7.3 HCO3 is 10X CO2 and 100X CO3
• Where does riverine HCO3 come from?
• How does the transport of HCO3 fit into the
terrestrial C balance?

69. Riverine HCO3 is soil respiration in
disguise
• The ultimate source of C in HCO3 is (mostly)
the atmosphere.
• Alkalinity comes from rock weathering which
either consumes atmospheric CO2 directly or
consumes CO2 from soil respiration.
• Terrestrial NEE (flux tower) is overestimated
by the amount of HCO3 lost

70. for carbonates
CO2 + H2O + CaCO3  Ca++ + 2HCO3
-
2CO2 + 2 H2O + CaMg (CO3)2  Ca++ + Mg++ + 4HCO3
-
Carbonate weathering – half the CO2 is atmospheric
for silicates
2 CO2 + 3 H2O + CaSiO3  Ca++ + 2 HCO3
- + H4SiO4
2 CO2 + 3 H2O + MgSiO3  Mg++ + 2 HCO3
- + H4SiO4
Silicate weathering – all the CO2 is atmospheric

71. Riverine HCO3 transport
units are Gt C y-1
• Total river DIC flux - 0.3 Gt y-1
• From carbonate weathering 0.14
• “atmospheric” C from carbonate
weathering 0.07
• From silicate weathering 0.15
• Total atmospheric C as DIC 0.22

72. Rivers – summary
units are Gt y-1
• CO2 efflux 0.15
• Organic C delivery 0.5
• Atmospherically derived
HCO3 (disguised soil R) 0.23
Burial – assumed ~ 0
Loss of terrestrial NEP in rivers 0.87
Note some organic C may be of riverine origin.

73. Nearly half of the “terrestrial” C sink is
in riverine transport.
• Net Terrestrial C sink 2-3 G t/y
• ___________________________
• Riverine transport 0.87
• Burial in lake sediments 0.05
• Reservoir burial 0.22
• ___________________________
• Freshwater components 1.14

74. 0
200
400
600
800
1000
1200
1400
1600
Terrestrial
Biomass Soil
Organic C stores on “land”OrganicC(Pg)

75. 0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Terrestrial pre-
industrial
Terrestrial, industrial
NetStorage(Pgy-1)
Annual Rates of net organic C
storage

76. -3
-2
-1
0
1
2
River
Flood plain
Ocean
abiotic
Terrestrial
biomass
increase
CO2flux(Pgy-1)
To atmosphere
from atmosphere
Note: pre-industrially biomass
increase approaches 0 and
ocean CO2 flux has opposite
sign

77. Ocean
Sediment storage
Inland waters
Ocean
Terrestrial NEP
(1-4 Pg C y-1)
Inland waters
CO2 evasion
0.90.9
0.91.9
0.75
0.23
Passive Pipe Model
Active Pipe Model
Cole et al. Ecosystems 2007

78. Ecosystem
• An ecosystem is defined as a spatially explicit unit
of the Earth that includes all of the organisms,
along with all components of the abiotic
environment within its boundaries – Likens 1992
• Boundary definition is a big problem! Ideally,
boundaries should represent the plane at which
short-term exchanges of matter are irreversible
relative to the functional ecosystem, ie, where
cycling becomes a flux. Likens et al. 1974

79. OXIDATION STATES OF SULFUROXIDATION STATES OF SULFUR
S has 6 electrons in valence shellS has 6 electrons in valence shell oxidation states fromoxidation states from ––2 to +62 to +6
H2SO4
Sulfuric acid
SO4
2-
Sulfate
+6
SO2
Sulfur dioxide
+4
FeS2
Pyrite
H2S
Hydrogen sulfide
(CH3)2S
Dimethylsulfide
(DMS)
CS2
Carbon disulfide
COS
Carbonyl sulfide
-2
H2SO4
Sulfuric acid
SO4
2-
Sulfate
+6
SO2
Sulfur dioxide
+4
FeS2
Pyrite
H2S
Hydrogen sulfide
(CH3)2S
Dimethylsulfide
(DMS)
CS2
Carbon disulfide
COS
Carbonyl sulfide
-2
Decreasing oxidation number (reduction reactions)
Increasing oxidation number (oxidation reactions)

80. THE GLOBAL SULFUR CYCLETHE GLOBAL SULFUR CYCLE
SO2
H2S
volcanoes industry
SO2
CS2
SO4
2-
OCEAN
1.3x1021 g S
107 years
deposition
runoff
SO4
2-
plankton
COS
(CH3)2S
microbes
vents
FeS2
uplift
ATMOSPHERE
2.8x1012 g S
1 week
SEDIMENTS
7x1021 g S
108 years