Presented by Eric A. Davidson at the Livestock Systems and Environment (LSE) Seminar, ILRI, Nairobi, 9 September 2014

1. Manure Happens: Altering the Global Nitrogen
Cycle by Feeding About Seven Billion Carnivorous
Humans
Eric A. Davidson
September 9, 2014

2. The History of Nitrogen
7,000
6,000
5,000
4,000
3,000
2,000
1,000
0
200
150
100
50
0
Invention of Haber Bosch Nitrogen
N-Discovered N-Nutrient BNF
N2 + H2
→ NH3
1750 1800 1850 1900 1950 2000 2050
Humans, millions Haber Bosch, Tg N

3. The Haber-Bosch process is
one of the greatest public
health boons in human history

4. The Fate of Haber-Bosch Nitrogen
N Fertilizer
Produced
N Fertilizer
Applied
N
in Crop
N
Harvested
N
in Food
N
Consumed
100 94 47 31 26 14
-6 -47 -12
-5
-16
14% of the N produced in the Haber-Bosch process enters the
human mouth……….

5. The Fate of Haber-Bosch Nitrogen
N Fertilizer
Produced
N Fertilizer
Applied
N
in Crop
N
Harvested
N
in Food
N
Consumed
100 94 47 31 26 14
-6 -47 -12
-5
-16
14% of the N produced in the Haber-Bosch process enters the
human mouth……….if you are a vegetarian.

6. People and Animals
7,000
6,000
5,000
4,000
3,000
2,000
1,000
0
250
200
150
100
50
0
1800 1850 1900 1950 2000 2050
Humans, millions Meat,Total
Millions of people
Millions of metric tons of meat
140 Manure-N
1860 1880 1900 1920 1940 1960 1980 2000
Nitrogen Inputs (Tg N yr-1)
120
100
80
60
40
20
0
Fertilizer-N
NOx-N

7. Increasing consumption of animal protein
Westhoek et al. (2011) “The Protein Puzzle”
Reay et al. (2011) European Nitrogen Assessment

8. The Fate of Haber-Bosch Nitrogen
N Fertilizer
Produced
N Fertilizer
Applied
N in
Crop
N in
Feed
N in
Livestock
N
Consumed
100 94 47 31 7 4
-6 -47 -3
-24
-16
4% of the N produced in the Haber-Bosch process and used
for animal production enters the human mouth.

9. Consumed
Animal
Products
N inputs:
synthetic N
fertilizers
manure
& natural N
fixation
Consumed
Crops
Nitrogen: A Very Leaky Element
NH3 N2O NOX N2
Crop
production
NH3 N2O NOX N2
Groundwater & surface waters
NH4
+ NO3
- DON Npart
NH4
+ NO3
- DON Npart
Atmosphere
feed
Agriculture
14%
4%
Animal
production

10. Natural N Fixation
N in Products
Energy
12%
Food
51%
Industrial
products
35%
Fiber
2%
Intentional N Fixation
Natural
19%
C‐BNF
29%
24.7 Tg N
Intentional
67%
Unintentional N Fixation
Unintentional
14%
Total N Fixation
Vehicles
63%
Utility and
Industry
35%
Other
2%
H‐B Fertilizer
46%
H‐B Industry
25%
Lightning
2%
BNF
98%
6.5 Tg N 4.8 Tg N
13.7 Tg N 23.3 Tg N
N lost to the Environment
N2O
3%
Hydrologic N
NOx
20%
NH3
13%
21%
Unknown
20 – 40%
N2
3 –23% Fates of intentional N
fixation in the U.S. for
2007. C-BNF = crop
biological N fixation;
H-B = Haber-Bosch.
Alteration of N Flows in the U.S.
• Intentional Nr creation accounts for 2/3rds
of total N2 fixation in the U.S.
• Nearly 2/3rds of unintentional Nr is from
vehicle use, while a majority of the
remainder is from stationary power plants
and industrial boilers.
• About 3/4ths of intentional Nr enters US
agricultural systems. Synthetic fertilizer
comprises 2/3rds of Nr input to U.S.
agriculture, with the remainder originating
from C-BNF. Industrial products like nylon
and explosives account for the remaining
25% of intentionally fixed Nr in the U.S.
• About 1/3rd of total Nr is incorporated into
products, about 1/3rd is lost as Nr to the
broader environment, about 1/3rd is
denitrified or lost to unknown sinks.
• Nitrogen use efficiency is about 38% for
agriculture and about 55% for all
intentional Nr.
From chapter by Benjamin Z. Houlton, Elizabeth Boyer,
Adrien Finzi, James Galloway, Allison Leach, Daniel
Liptzin, Jerry Melillo, Todd S. Rosenstock, Dan Sobota,
and Alan R. Townsend
Biogeochemistry (2013) 114:11-23

11. The upper photo shows a site in Southern California
dominated by exotic annual grasses five years after a burn,
and the lower shows a site immediately post-burn.
Climate-N Interactions and
Biodiversity
 Both empirical studies and modeling
indicate that N and climate change
can interact to drive losses in
biodiversity greater than those
caused by either stressor alone.
 In arid ecosystems of southern
California, elevated N deposition and
changing precipitation patterns have
promoted the conversion of native
shrub communities to communities
dominated by a few species of
annual non-native grasses.
 A change in biodiversity can also
affect ecosystem function, such as
increasing fire risk where fuel
accumulation was previously rare.
From chapter by E. Porter, W. D.
Bowman, C. M. Clark, J. E. Compton, L.
H. Pardo and J. Soong
Biogeochemistry 114: 93-120
Photos by Edith Allen

12. Reactive N in the atmosphere causes several
forms of air pollution (as well as the GHG N2O)
 O3
 Fine Particulate Matter (PM2.5)
 NO2
EPA 2005 estimates for US:
• PM2.5 exposure caused 130,000 annual
premature deaths
• Ozone exposure caused another 4,700
annual premature deaths .
• Hundreds of thousands of hospital
visits and millions of additional
respiratory symptoms each year are
also attributed to this pollution

13. Drinking Water Nitrate
 U.S. standard of 10 ppm
 In place because of
methylglobinemia
 The need for
maintaining the
standard is a matter of
recent controversy
Methemoglobinemia
“blue baby syndrome”

14. Davidson et al. 2012. Issues in Ecology, Report
Number 15, Ecological Society of America.
WHO International
Agency for Research on
Cancer expert working
group:
 “ingested nitrate or
nitrite under
conditions that result
in endogenous
nitrosation is probably
carcinogenic to
humans”
 NOCs are potent
carcinogens and
teratogens in animals
including non-human
primates.

15. Birth defect risks
 Prenatal exposure to
nitrate in drinking water
is associated with neural
tube defects, oral cleft
defects, and limb
deficiencies.
 These birth outcome
risks occurred at
exposures below the
current MCL for public
water supplies.
 However, nitrate may
occur in conjunction
with other contaminants
(e.g., arsenic,
pesticides).

16. USGS findings for 2001-2004:
• The federal MCL drinking-water
standard was exceeded
in >20% of shallow (<30m
below the water table)
domestic wells in agricultural
areas, an increase from 16% a
decade earlier.
• About 1.2 million Americans
use private drinking wells
with [NO3-] between 5 and 10
mgN L-1 and about 0.5 million
use wells that exceed 10 mgN
L-1.
• The [NO3-] in deep
groundwater increased from
1.2 to 1.5 mgN L-1, indicating
that municipal water sources
may be at risk in the future.
Davidson et al. 2012. Issues in
Ecology, Report Number 15,
Ecological Society of America.

17. Hog production
NH3 emissions
Costal
eutrophication
Grain production

18. Hypoxic Zones & Eutrophic Coastal Area
http://www.vims.edu/research/topics/dead_zones/

19. A German family with food for one week AA Sno Ammaeliraicnafna mfaimlyi lwyi twhi tfho ofodo fdo rf oorn oen we eweekek
Hungary Planet: What the World Eats
Faith D'Aluisio and Peter Menzel, Random House, 2005

20. NATURE|Vol 461|24 September 2009
“Editor’s note Please note that this
Feature and the Commentaries are not
peer-reviewed research. This Feature,
the full paper and the expert
Commentaries can all be accessed from
http://tinyurl.com/planetboundaries.”

21. EPA. 2006. Global Anthropogenic Non-CO2 Greenhouse Gas
Emissions: 1990-2020.

22. Crutzen et al. Atmos. Chem. Phys. 8, 389-395 (2008)
Pre-industrial:
Stratospheric photochemical sink of N2O  total N2O source  10.2 TgN2O-N/yr
Natural source from land and coastal zones = 6.2 to 7.2 TgN2O-N/yr
New annual N fixation = 141 Tg N/yr
N2O yield = 6.2 to 7.2 TgN2O-N/yr  141 Tg N/yr “new” fixed N
= 4.4 – 5.1%
1990-2000
Stratospheric photochemical sink of N2O: 11.9 TgN2O-N/yr
Total N2O source = photochemical sink (11.9 TgN2O-N/yr) + atmospheric growth
(3.9 TgN2O-N/yr) = 15.8 TgN2O-N/yr
Anthropogenic N2O source = total source (15.8 TgN2ON/yr) - current natural source
(9.3 to 10.2 TgN2O-N/yr) = 5.6–6.5 TgN2O-N/yr
Agricultural contribution = 5.6–6.5 TgN2O-N/yr - industrial source (0.7–1.3
TgN2O-N/yr) = 4.3–5.8 TgN2O-N/yr
New anthropogenic fixed N = 86 Tg N Haber-Bosch fertilizer + 24.2 Tg N fixed due
to fossil fuel combustion + 3.5 Tg new BNF = 114 Tg N/yr
Anthropogenic N2O yield = 4.3–5.8 TgN2O-N/yr  114 Tg N/yr “new” fixed N
= 3.8 – 5.1%

23. 320
Atmospheric N 2O (ppb) Observed
310
300
290
280
270
Crutzen model
1860 1880 1900 1920 1940 1960 1980 2000
The Crutzen et al. (2008) model, based on 4% of annual newly fixed
N, underestimates atmospheric N2O from about 1880 to 1980.
To match the observed rate of atmospheric accumulation in the
1950s, 10% of annual newly fixed N would have to have been
converted to N2O. Davidson, E.A. 2009. Contribution of manure and fertilizer nitrogen to
increasing atmospheric nitrous oxide since 1860. Nature Geoscience,
2:659-662.

24. 320
310
300
290
280
270
1860 1880 1900 1920 1940 1960 1980 2000
Atmospheric N 2O (ppb)
Observed
Crutzen model
160
140
120
100
80
60
40
20
0
1860 1880 1900 1920 1940 1960 1980 2000
Nitrogen (Tg/year)
Manure
Synthestic N Fertilizer
NOx
Holland, E. A., Lee-Taylor, J.,
Nevison, C., & Sulzman, J.
Global N cycle: fluxes and N2O
mixing ratios originating from
human activity. Data set
available on-line
[http://daac.ornl.gov/CLIMATE/g
uides/N_Emiss.html] from Oak
Ridge National Laboratory
Distributed Active Archive
Center, Oak Ridge, Tennessee,
U.S.A. (2005).

25.  Time-course analysis of sources and sinks of atmospheric N2O since 1860,
using both top-down and bottom-up constraints
 Previously compiled database (Holland et al. 2005) of:
• atmospheric N2O concentrations
• manure production
• fertilizer-N use
• legume cultivation
• NOx emissions
 New annual estimates of N2O production from:
• fossil fuel N2O sources
• nylon production
• biomass burning
• tropical deforestation
• temporal estimates of the stratospheric sink for N2O

26.  For each year, the anthropogenic biological source was
calculated as follows:
 Anthro-Bio source = Atmospheric growth – industrial
& transport sources + anthropogenic sink + reduced
natural tropical forest soil source
 The fractions of annual manure-N production (Fm) and
annual synthetic fertilizer-N production (Ff) that are
released as N2O were estimated by multiple linear
regression, using historical data for manure-N and
fertilizer-N production:
 Anthro-Bio source = Fm*manure-N + Ff*fertilizer-N

27.  Anthro-Bio source = 0.0203*manure-N + 0.0254*fertilizer-N
(p < 0.0001 for each coefficient; adjusted R2 = 0.98)
 The entire 19th-20th century pattern of increasing atmospheric N2O
can be fit to a regression model related to human food production
systems, assuming that 2.0% of annual manure production and 2.5%
of annual synthetic fertilizer-N production are released as N2O.
 Sensitivity analyses of uncertainties in input data suggest that these
coefficients likely fall within these ranges:
 Manure-N production: 1.6% - 2.7%
 Fertilizer-N production: 1.7% - 2.7%
 These yield percentages are within the ranges of uncertainty of IPCC
average emission factors.
 However, these results differ from the Crutzen et al. (2008) model,
because manure-N is not necessarily newly fixed N.

28. Atmospheric N2O-N Growth (TgN/yr) Total Source Model
6
5
4
Manure
3
was the
dominant
2
source in
1
the 19th
century 0
NylonN2O
TransportN2O
FertilizerN2O
ManureN2O
Biomass Burning
1860 1880 1900 1920 1940 1960 1980 2000
Manure
still
dominates,
but
fertilizers
are also
important

29. Where does the N in manure
come from? It may not all be
newly fixed N.
Mining of soil N due to
expansion of livestock and
agricultural production from
1860 to 1960, before synthetic
fertilizer-N could replace lost
soil N, could explain why
atmospheric N2O increased
from 1860 to 1960 at a faster
rate than predicted from a
model of 4% of annual new N
fixation.
David, M. B., McIsaac, G. F., Royer, T. V., Darmody,
R. G. & Gentry, L. E. Estimated historical and
current nitrogen balances for Illinois. The
Scientific World 1, 597-604. DPO
10.1100/tsw.2001.283 (2001).

30. Units are Gg N yr-1
David, M. B., McIsaac, G. F., Royer, T. V.,
Darmody, R. G. & Gentry, L. E. Estimated
historical and current nitrogen balances for
Illinois. The Scientific World 1, 597-604. DPO
10.1100/tsw.2001.283 (2001).

31. http://www.unep.org/publications/ebooks/
UNEPN2Oreport/

32. What are the technical, economic, and social impediments
and opportunities for increased nitrogen use efficiency in
crop and animal production systems?

33. Nitrogen Use Efficiency in
Nebraska’s Central Platte
Valley
Richard B. Ferguson
Hog production
NH3 emissions
Professor of Soil Science
Costal
eutrophication
Department of Agronomy & Horticulture
University of Nebraska-Lincoln
Grain production

35. Stakeholder input on
performance
indicators
They have power -
ballot box and the
super market
Paul Fixen
Applying the Right Source at the Right Rate at the Right Time and in the Right
Place, where Right is defined by practice impact on system performance

36. Trends in the Central Platte Valley
y = ‐0.1523x + 321.41
R² = 0.824
y = ‐2.1092x + 4289.4
R² = 0.6312
20
19
18
17
16
15
14
13
12
11
Average of values from producer reports in GWMA, representing ~ 300,000 acres
200
180
160
140
120
100
80
60
40
20
0
10
1985 1990 1995 2000 2005 2010 2015
Soil Residual NO3‐N (lb/acre)
Groundwater NO3‐N(ppm)

37. Balanced
rations
Total mix-ed
rations
bST
Milk 3x/d
A study of 54 dairy farms in Wisconsin demonstrated that more of the N fed
to cows ends up in the milk and less in the manure when:
• the feed is modified to be more balanced
• hormones are managed
• when milking is done three times per day.
Adapted from Powell et al. 2006. J. Dairy Sci. 89,2268-2278

38. Estimated shares of variable costs per
acre for rotation corn in Indiana in 2013
Mixed economic signals
From 2013 Purdue Crop Cost &
Return Guide. Purdue Extension
publication ID-166-W.
 N fertilizer costs are high enough for many farmers to want to
improve NUE.
 But most also agree that the economic risk of applying too little N
is high.
 N application provides an important economic margin of safety, like
relatively inexpensive insurance.

39. Estimated costs for adopting several currently available management practices across the
Ceder Creek Watershed, Iowa, for a 35% load reduction, implemented over a 20 year period.
The total cost is $71 million per year, or $7.78 kg-1 N removed yr-1, or $42 ha-1 yr-1 (from Dan
Jaynes, USDA-ARS, and Mark David, Univ. Illinois).
Davidson et al. 2012. Issues in Ecology, Report Number 15, Ecological Society of America.

40. RECOMMENDATIONS:
 Develop partnerships & networks between industry,
universities, governments, NGOs, crop advisors, and
farmers to demonstrate the most current, economically
feasible, best management practices.
 Provide improved, continuing education to private sector
retailers and crop advisors through professional
certification programs by university and government
extension
 Provide science-based recommendations through trusted
sources of information to help reduce the perception of
risk and the perceived need to apply additional N Linda for
Prokopy
“insurance” purposes.
Purdue Univ.

41. PAN AFRICAN SOIL NUTRIENT DEPLETION
1995-97 2002-04
Source: IFDC
kg nutrient ha-1

42. Initial Goal of African Green Revolution
Moving from 1 to 3 tons per hectare
0 N added
1 ton/ha of maize
50 kg N ha-1
3 tons/ha maize