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A brief history of phosphorus: From the philosopher’s stone to nutrient recovery
and reuse
K. Ashley
a,
⇑
, D. Cordell
b
, D. Mavinic
a
a
Department of Civil Engineering, Faculty of Applied Science, University of British Columbia, 6250 Applied Science Lane, Vancouver, BC, Canada V6T 1Z4
b
Institute for Sustainable Futures, University of Technology, Sydney, PO Box 123 Broadway, NSW 2007, Australia
article info
Article history:
Received 12 October 2010
Received in revised form 28 February 2011
Accepted 1 March 2011
Available online 8 April 2011
Keywords:
Green Revolution
Historical analysis
Eutrophication
Peak phosphorus
Phosphorus cycle
Sanitation Revolution
abstract
The element phosphorus has no substitute in sustaining all life and food production on our planet. Yet
today’s phosphorus use patterns have resulted in both a global environmental epidemic of eutrophication
and led to a situation where the future availability of the world’s main sources of phosphorus is uncer-
tain. This paper examines the important history of human interference with the phosphorus cycle from
initial discovery to present, highlighting key interrelated events and consequences of the Industrial Rev-
olution, Sanitation Revolution and Green Revolution. Whilst these events led to profound advances in
technology, public health and food production, they have fundamentally broken the global phosphorus
cycle. It is clear a ‘Fourth Revolution’ is required to resolve this dilemma and ensure humanity can con-
tinue to feed itself into the future while protecting environmental and human health.
Ó2011 Elsevier Ltd. All rights reserved.
1. Introduction
The prominent chemist and science writer Isaac Asimov suc-
cinctly stated: ‘‘Life can multiply until all the phosphorus has gone
and then there is an inexorable halt which nothing can prevent’’
(1974). The element phosphorus is essential to all life – plants, ani-
mals and bacteria. This means phosphorus has no substitute in
growing crops and hence in food production. Yet, today’s phospho-
rus use patterns in the global food production and consumption
system have resulted in a global environmental epidemic of fresh-
water eutrophication and marine ‘dead zones’ (World Resources
Institute, 2008) and simultaneously led to a situation where the fu-
ture availability of the world’s main sources of phosphorus are
uncertain (Cordell et al., 2009).
Understanding the history of human-based phosphorus use can
shed light on how we arrived at this unsustainable situation today,
and assist in developing innovative solutions for future sustainable
use of phosphorus. The story of phosphorus began with the
alchemists search for the Philosopher’s Stone, and centuries later,
the critical role of phosphorus in soil fertility and crop growth
was highlighted. Eventually, phosphorus was identified in the glo-
bal environmental problem of eutrophication. Now, we are on the
brink of yet another emerging chapter in the story: global phos-
phorus scarcity linked to food security (Fig. 1). This paper examines
the important history of human interference with the phosphorus
cycle from initial discovery to present, highlighting key interre-
lated events and consequences of the Industrial Revolution, Sanita-
tion Revolution and Green Revolution.
2. The elemental discovery of phosphorus
Phosphorus has been a defining element throughout modern
human history. The elemental form was discovered around 1669
by the German alchemist Hennig Brandt. Earlier origins are a mys-
tery, as phosphorus may have been discovered in ancient Rome,
then its secret lost through the ages (Emsley, 2000). In his Ham-
burg laboratory, Brandt distilled 50 buckets of urine through in-
tense heating and distillation in search of the legendary
‘Philosopher’s Stone’ that would supposedly turn base metals into
gold (Emsley, 2000). His recipe was simple, yet effective (Ogilvy,
2006):
Boil urine to reduce it to a thick syrup.
Heat until a red oil distills up from it, and draw that off.
Allow the remainder to cool, where it consists of a black spongy
upper part and a salty lower part.
Discard the salt, mix the red oil back into the black material.
Heat that mixture strongly for 16 h.
First white fumes come off, then an oil, then phosphorus.
The phosphorus may be passed into cold water to solidify.
0045-6535/$ - see front matter Ó2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.chemosphere.2011.03.001
⇑
Corresponding author. Address: 1957 Westview Drive, North Vancouver, BC,
Canada V7M 3B1. Tel.: +1 604 987 6290.
E-mail address: ken.ashley@shaw.ca (K. Ashley).
Chemosphere 84 (2011) 737–746
Contents lists available at ScienceDirect
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
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Whilst he found no such magical stone capable of transmuta-
tion, Herr Doktor Brandt discovered the pure form of phosphorus,
which also glowed in the dark. A slow chemical reaction with
atmospheric oxygen occurs at the surface of the solid (or liquid)
phosphorus, which forms short-lived molecules of HPO and P
2
O
2
,
both of which emit a faint green glow in the visible spectrum (Ems-
ley, 2000)(Fig. 2). Ironically, this same essential reaction is still
used today, but with mined phosphate ores, coke for carbon, and
electric furnaces.
After much secrecy, Brandt revealed the existence of phospho-
rus in 1675, and his fellow alchemist Daniel Kraft generated fame
and income entertaining European nobility by demonstrating this
mysterious new source of light. The name phosphorus is derived
from the Greek ‘phôs’ meaning ‘‘light’’, and ‘phoros’ meaning
‘‘bearer’’, the same name given by ancient Greek and Roman
astronomers to the planet Venus, when it appeared in the sky as
the morning star (Vallentyne, 1974). By 1676 Johann Kunckel
was able to make phosphorus, followed in 1680 by Robert Boyle
in London (Emsley, 2000). Antoine Lavoisier (founder of modern
chemistry) finally recognized phosphorus as an element a century
after Brandt’s discovery (Emsley, 2000).
The main use of phosphorus in the 17th and 18th centuries, fol-
lowing its chemical isolation by Brandt, was for highly question-
able medicinal purposes. However, the discovery in the late 18th
century that bones were a more abundant source of mineral phos-
phorus than urine, led to the mass manufacturing of phosphorus
matches, and emergence of the gruesome occupational hazard of
‘phossy jaw’ (Emsley, 2000). White phosphorus was a dangerous
element that could now be produced in relatively high quantities.
As an elemental form of phosphorus, white phosphorus is highly
reactive and hence not found in nature. It is flammable when ex-
posed to air, can spontaneously combust and is a deadly poison
in low doses (Emsley, 2000). Phosphorus became known as the
‘Devil’s element’, due to its life-destroying properties when used
in military applications (such as artillery shells, tracers, grenades,
smoke cartridges, and fire bombings) and in organophosphate bio-
cides. The most potent of these was the nerve gas VX, which is
lethal at 0.1 mg per kg of body weight when applied to exposed
skin (Emsley, 2000). By the 20th century it was a common ‘element
of war’ and Emsley notes the tragic irony that 2000 tonnes of
‘‘burning phosphorus’’ was used in ‘Operation Gomorrah’ to bomb
Hamburg and create a horrific firestorm during one summer week
in World War II.
Phosphorus is an unusual element. It is not found in nature as a
free element due to its high reactivity, yet it has several allotropes,
the most common being the white, red and black forms. Allotropes
are different elemental arrangements of atoms with vastly differ-
ent properties; carbon being a well-known example with diamond,
graphite and fullerene allotropes. The red and white forms of phos-
phorus are both insulators, and of nonmetallic character, whereas
the black form has a crystal structure made up of corrugated
sheets, and behaves like a semi-metal (Mahan, 1969). Phosphorus
has two radioactive beta-emitting isotopes,
33
P and the higher en-
ergy
32
P(Winter, 2010). Unlike the other major elements of life
(i.e., C, H, O and N), phosphorus does not have a gaseous phase
and cannot circulate freely in the atmosphere. As will be discussed
later, this has very important implications with respect to phos-
phorus recovery and reuse.
Biochemically, phosphorus is the basis for all life on our planet.
Adult humans contain approximately 0.7 kg of phosphorus, mainly
in bones and teeth as calcium phosphate salts. At the molecular le-
vel, in the polynucleotide structures DNA and RNA, phosphorus
forms the phosphodiester bridges that link one nucleotide to the
next. Adenosine triphosphate (ATP) is the primary carrier of
chemical energy in cells, via transfer of phosphate groups from
energy-yielding to energy-requiring processes. Phospholipids,
which contain phosphorus in the form of phosphoric acid, are
found in cellular membranes and in the lipoproteins of blood
plasma (Lehninger, 1973).
In the biosphere, animals obtain phosphorus from food (plants
or lower trophic-level animals); plants, in turn, obtain phosphorus
Fig. 1. The evolution of phosphorus use and abuse: from the Philosopher’s Stone to use in war, food production, and more recently implicated in water pollution. A new
emerging discourse of the 21st century may be global phosphorus scarcity. Source:Cordell (2010).
Fig. 2. ‘‘The Alchymist, In Search of the Philosopher’s Stone’’. Henning Bandt’s
chemical discovery of phosphorus in 1669. Painting: Joseph Wright.
738 K. Ashley et al. / Chemosphere 84 (2011) 737–746
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from soils (Johnston, 2000). Mineral sources of soil phosphorus
originally come from rock containing phosphorus-rich apatite, that
has taken around 10–15 million years to form (White, 2000). These
sources started their life as remains of aquatic life (such as shells).
They were eventually buried on the sea floor, and transferred to the
lithosphere via mineralisation and tectonic uplift over millions of
years and eventually weathered down, via wind and rain erosion.
Plants require phosphorus for cell growth, the formation of
fruits and seeds and ripening (Johnston, 2000). Hence, plant phos-
phorus deficiencies can severely hinder crop yields and fruit/seed
development. While phosphorus is highly abundant in nature, it
is one of the least biologically available nutrients. That is, the forms
in which it exists in the biosphere are often ‘unavailable’ for plants.
Plants can only absorb the soluble inorganic form of phosphorus
(known as orthophosphates) dissolved in soil solution.
3. Phosphorus cycling in historical food systems
Historically, humans relied on natural levels of soil phosphorus
for crop and food production, with additions of organic matter like
manure and crop residues. Societies developed regional or local
methods of food production that suited the landscape, climate
and culture; however, food was always produced and consumed
locally.
As long as 40 000 years ago, before agrarian societies developed
such practices, hunter-gatherers (such as Aboriginal people in Aus-
tralia) used ‘firestick’ farming, which largely ceased after European
settlement in Australia in the late 1700’s. Through localized and
controlled patchwork burning, they manipulated the environment
to increase the productivity of edible plants and animals while
simultaneously reducing fuel build up that could otherwise lead
to dangerously intense wildfires (Cordell, 2001). Australian soils
are naturally low in phosphorus, and fire converts unavailable
phosphorus bound in soil and plant matter into an inorganic form
in ash, temporarily available to plant roots. In addition to increas-
ing the temporary bioavailability of nutrients, patchwork burning
also increased availability of edible plants and animals by creating
micro-ecosystems of vegetation communities of different ages to
increase diversity and possibly local carrying capacity. Further,
burning under-story vegetation would expose animals, increasing
the ease of hunting. Indirectly, the sudden regeneration initiated
by fire would also attract grazing animals such as kangaroos and
wallabies which could be hunted (Cordell, 2001). In this way, such
burning practices played a vital role in sustaining Aboriginal com-
munities over tens of thousands of years (Flannery, 1994; Flood,
1999).
The use of anthropogenic fire to recycle nutrients accelerated
the emergence of agriculture in Europe, as the practice evolved
from fire herding of animals to fire-assisted farming. The Neolithic
observations that plants blossomed on burned sites, eventually led
to the development of the rotational style of European agriculture,
based on the use of fire to release calcium, potash and phosphorus,
and to control the succession of vegetation on the site. This type of
fire-fallow, slash-and-burn style of rotational agriculture has been
termed ‘swidden’ (Pyne, 1997).
In rural Asia (particularly China), the use of human excreta –
‘night soil’ – in the fields has been common practice for at least
5000 years (Mårald, 1998). Victor Hugo even observed in Les
Miserables:
Science, after having long groped about, now knows that the
most fecundating and the most efficacious of fertilizers is
human manure. The Chinese, let us confess it to our shame,
knew it before us. Not a Chinese peasant goes to town without
bringing back with him, at the two extremities of his bamboo
pole, two full buckets of what we designate as filth. Thanks to
human dung, the earth in China is still as young as in the days
of Abraham. Chinese wheat yields a hundred fold of the seed
(Hugo, 1862).
Chinese aquaculture, or more appropriately polyculture, has
also been based for millennia on the recycling of manure from
domesticated animals. Animal droppings either fell directly into
or were added to fish ponds, to promote algae and zooplankton
growth. This yielded high biomasses of herbivorous and/or plank-
tivorous species of fish. This sustainable approach to protein pro-
duction independently emerged in the Danube basin and carp
culture has been practiced throughout Central and Western Europe
since the Middle Ages (Neess, 1949; Hoffman, 1995).
A common practice in the Middle East around 1st century BC–
1st century AD during Roman and Byzantine Era’s was to keep pi-
geons not only for meat, but for their manure, a fertilizer rich in
phosphorus. Archeological evidence suggests that societies in the
Nile region in Egypt and desert regions of southern Israel kept
pigeons in columbarium towers (such as that pictured in Fig. 3)
(Tepper, 2007). The pigeons were likely free to forage for food
among refuse piles and wild desert flora, in addition to being fed
some agricultural crop residues and seeds (Ramsay and Tepper,
2010). Tepper (2007) estimates that a columbarium tower, con-
taining 1000 pigeon nesting cells, would have been able to supply
approximately 12 tonnes of fertilizer a year, enough to fertilize
around 1500 fruit trees and a small garden. Soil fertility of agricul-
tural fields in such desert areas was improved, not only with pi-
geon manure, but other organic sources of nutrients, such as cow
and goat manure, crop and food residues, ash and even furniture
(Tepper, 2007). The phosphorus in Nile agriculture originated from
annual flooding of the Nile, and ultimately came from erosion in
the headlands, hence the role of geologic erosion and periodic
flooding must be acknowledged in the renewal of soil fertility
(Nixon, 2004).
In Japan, during the Edo era (1603–1868), the residents of early
Tokyo supported a population of over 500 000 residents by care-
fully recycling their human and animal wastes, and small marine
fish, back to their agricultural fields (Cederholm et al., 1999;
Vaccari, 2011). Edo era, wood block carvings show farmers carrying
night soil back to the fields and collecting guano from nearby bat
caves. Upland erosion likely provided an additional source of phos-
phorus in pre-industrial Japan.
In medieval England, it was common practice for nobility to
allow peasants to graze sheep on Lord’s Land, but they faced
severe punishment if caught removing sheep droppings. This
Fig. 3. Remains of ancient dovecotes towers found on Masada, Israel (circa 60–70
AD) used for housing pigeons for meat and fertilizers. This was thought to be
essential for survival atop the isolated desert plateau. Photo: Dana Cordell.
K. Ashley et al. / Chemosphere 84 (2011) 737–746 739
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demonstrated an uncanny appreciation for the critical role of phos-
phorus recycling in early agriculture (Driver et al., 1999). The car-
rying capacity of the British Isles was only five million people in
the Middle Ages, whereas the current population is 55 million,
the difference due to the importation of mineral phosphorus for
agriculture and food for direct consumption (Emsley, 2000).
Whilst these past communities would not have known about
the chemical properties of phosphorus, their ability to maintain
soil fertility through organic matter and fire underpinned their
very survival.
4. The Sanitation Revolution and consequences for the
phosphorus cycle
The development of human settlements, and in particular sani-
tation arrangements, fundamentally changed the global phospho-
rus cycle.
In medieval Europe, cities initially began as an attempt to ward
off outside threats. At first, the distances between agricultural
fields and cities were minor, and the cities ‘night soil’ could be
transported back to the agricultural land to maintain soil produc-
tivity. However, the Industrial Revolution (1760) triggered mass
movement of European populations to cities of unprecedented
size. The Industrial Revolution started in 1760 in the UK, with
the replacement of animal energy with fossil fuels (initially with
coal, then cheap hydrocarbons and hydroelectricity) and the
migration of workers to cities, which started a world-wide transi-
tion to an industrialized manufacturing economy. As cities grew,
they developed their own internal threats: namely crime, fire
and disease. By 1854 London was among the world’s largest cities
– 2.5 million people packed inside a 20 km circumference. This had
rarely been done before, and it was uncertain if cities this large
were sustainable: a bustling Victorian metropolis saddled with
Elizabethan public infrastructure (Johnson, 2006). The living condi-
tions in Victorian London were abysmal: 700 000 chimneys and
2000 steam engines – all running on coal, and disease, death
and illness were omnipresent. London air was ‘‘a compound of
fen fog, chimney smoke, smuts and pulverized horse dung’’ – it
killed 3000 people in 1879–80 (McNeill, 2000).
The most noticeable feature of Victorian London was the smell
of decomposing organic matter (Johnson, 2006). Communicable
disease outbreaks increased with the growing population density.
The London plague epidemic in 1665–66 killed 60 000; cholera
killed 14 137 in 1849 and 10 738 in 1853. Disease was believed
to spread via foul odours – the ‘miasma’ theory. London’s huge
sprawl restricted the removal of waste. Night soil men typically
worked the graveyard shift in teams of four: a ‘‘ropeman’’, a ‘‘hol-
eman’’ and two ‘‘tubmen’’. The flushing toilet was invented by Sir
John Harrington in 1596; however, the 1775 and 1778 patents,
by Alexander Cummings and Joseph Bramah for the modern flush
toilet, compounded the waste disposal problem by regular flooding
of numerous cesspools in London (Johnson, 2006). Most houses
just let sewage accumulate in backyard cesspools, or house base-
ments. London’s few sewers were only carrying cesspool runoff
and surface runoff a short distance to the Thames River. Now,
‘‘night soil’’ was no longer returned to the land as the tonnages
and distances were too large; a pervasive fear of bad smells re-
mained, due to foul odours from mass graveyards and sewers.
The turning point occurred on August 28, 1854 when fouled
water from the daughter of Thomas and Sarah Lewis was disposed
in the cesspool in front of their house. This started the 1854 out-
break of cholera in London – the famous ‘‘Broad Street Pump’’ inci-
dent which killed 616 people. Over the next few weeks, Dr. John
Snow and Rev. Henry Whitehead conclusively demonstrated the
source of infection was the Broad Street well contaminated by
wastewater from the adjacent cesspool, culminating with the dra-
matic step of removing the handle from the pump. This event rep-
resented an important milestone in the ‘Sanitary Revolution’ and
the founding event in the new science of public health epidemiol-
ogy (Johnson, 2006).
Slow sand filtration for water supplies, invented in 1830, rap-
idly expanded after the Broad Street Pump incident. The massive
London sewer system of 120 km of interceptor sewers and
720 km of main sewers was finally built between 1859 and 1865,
under the direction of Sir Joseph Bazalgette. The science of bacteri-
ology originated soon afterwards from 1862 to 1870s due to the
pioneering efforts of Louis Pasteur and Robert Koch. Emergency
chlorination of water supplies had been practiced since about
1850, and continuous chlorination of potable water supplies
started in England in 1904 as the principles of public health and
sanitation became firmly established in western countries (Sawyer
and McCarty, 1978).
The ‘Sanitation Revolution’ transition from land based to water-
based disposal of human wastes fundamentally changed 19th and
20th century civilization, from a phosphorus recycling society to a
phosphorus through-put society (Fig. 4). Mineral phosphate, now
widely available, was used once, and then discarded in one pass
water-based disposal systems. ‘‘Night soil’’ was no longer returned
to the land in most European and North American cities, as the ton-
nages and distances became too large; public health concerns and
the expanding Industrial Revolution economies mandated safe dis-
posal, rather than reuse.
5. The Green Revolution and humanity’s dependence on
phosphate rock
Following the Industrial and Sanitation Revolutions, the next
Revolution was to have a profound impact on the phosphorus cycle
– the Green Revolution that reformed agriculture and largely aban-
doned organic fertilizers.
Popular thought in Europe until mid-19th century was that that
plants and animals were given life in a mysterious way, from dead
and decomposing plants and animals. It was not until 1840 that
Justus von Liebig (founder of organic chemistry) confirmed the fer-
tilizing effect of humus on plant growth was due to inorganic salts
of phosphorus and nitrogen, and not organic matter (Liebig, 1840).
Liebig’s ‘mineral theory’ provided a scientific explanation of how
nutrients like phosphorus, nitrogen and potassium were essential
elements that circulated continuously between dead and living
matter. Despite its radical nature, this theory was widely adopted
in Western agriculture and practices were adapted accordingly.
Increasing soil degradation and famines in Europe in the 17–
18th centuries triggered a search for external sources of fertilizers
to boost crop yields (Mårald, 1998; Emsley, 2000). England, for
example, imported large volumes of crushed bones (rich in calcium
phosphate) from mainland Europe to apply to British farmlands.
The same took place in the US (Fig. 5). This was later taken one step
further by dissolving bones in sulfuric acid, to create a liquid fertil-
izer (Liu, 2005; Rothamsted Research, 2006).
Around the same time, concentrated mineral sources of phos-
phorus were discovered in guano (bird and bat droppings) off the
coast of Peru, and on islands in the South Pacific, such as Nauru
and Christmas Island. In 1856, the US Congress passed the ‘Guano
Islands Act’ to facilitate access to uninhabited islands in the Pacific
and Atlantic that held significant guano reserves. Phosphate rock
deposits rich in phosphate were also identified in the US (Brink,
1977; Smil, 2000). Sir Joseph Henry Gilbert (who had studied under
Liebig) and Sir John Bennet Lawes together founded the Rotham-
sted Research in 1840’s in England, to undertake long-term trials
of the effectiveness of mineral and organic fertilizers on crop yields
740 K. Ashley et al. / Chemosphere 84 (2011) 737–746
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(Rothamsted Research, 2006). Eventually, it was demonstrated that
more phosphorus needed to be applied to fields than the amount
removed in harvest crops.
However, it was not until the post-World Water II period that
use of mineral phosphorus sources grew exponentially (Fig. 6).
Phosphate rock was seen as a cheap and plentiful source of phos-
phorus and it became widely used in favour of organic sources
(Brink, 1977; Smil, 2000). To keep up with rapid population
growth, increasing food shortages and urbanization in the mid-
20th century, high-yielding crop varieties were developed, known
as the Green Revolution. This was supported by the invention of
the Haber–Bosch process, which allowed the production of high
volumes of artificial nitrogenous fertilizers, with external inputs
of irrigation water, nutrients, pesticides, herbicides and hydrocar-
bon energy, rather than manual labour (Brink, 1977; Fresco,
2009). Phosphate rock was now mined to keep up with nitrogen
fertilizer demand. Fertilizer use sextupled between 1950 and
2000 (IFA, 2006). The Green Revolution contributed to the doubling
of crop yields and increasing per capita nutritional intake (IFPRI,
2002).
While phosphate rock seemed like limitless source of highly
concentrated phosphorus, it was relying on a non-homogenous,
non-renewable resource. Today, societies are effectively dependent
on phosphorus from mined phosphate rock. Without continual in-
puts, we could not produce food at current global yields (Cordell,
2010).
There is little doubt today of the importance of additions of
mineral phosphorus fertilizers in producing food at current global
yields. Indeed, phosphate rock, together with nitrogen and potas-
sium fertilizers, and relatively inexpensive hydrocarbon fuels,
were responsible for feeding billions of people over the past cen-
tury. The need to raise soil fertility in nutrient deficient areas like
Fig. 4. Evolution of sanitation throughout human history, from ‘Early civilization and the middle ages Era’, to the ‘sanitary awakening and advent of water-borne sanitation
era’, through to the ‘waste water reclamation and eutrophication control Era’, and possible future ‘Ecological sanitation Era’. Source: Redrawn from Gumbo (2005).
K. Ashley et al. / Chemosphere 84 (2011) 737–746 741
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Sub-Saharan Africa is relatively well understood by the food
security community. However, few discussions have explicitly
addressed the emerging challenge of where and how phosphorus
will be obtained in the future, to ensure continuous food availabil-
ity for a growing world population.
6. The nutrient cycle is broken
The Green Revolution and Sanitation Revolution both had pro-
found consequences on the global phosphorus cycle. While indus-
trialized agriculture established a dependence on mined phosphate
rock in favour of organic sources, water-based disposal of human
wastes fundamentally changed modern civilization from a phos-
phorus recycling society to a phosphorus through-put society.
Today, phosphorus is mined in only a few geographical locations,
processed into fertilizers and transported around the globe to ap-
ply to the world’s agricultural fields. Unlike the natural biochemi-
cal cycle, which recycles phosphorus back to the soil via dead plant
matter, industrial agriculture harvests crops prior to their decay
phase and transports them all over the world for food production
and consumption. This means continual applications of phospho-
rus-rich fertilizer are required to replace the phosphorus that is re-
moved from the soil when crops are harvested. Once consumed,
most phosphorus molecules in food exit our bodies in urine
(70%) and faeces (30%) – approximately half a kilogram per person
each year (Jönsson et al., 2004). As early as 1928, Aldus Huxley
wrote in ‘‘Point Counter Point’’:
‘‘With your intensive agriculture...you’re simply draining the
soil of phosphorus. More than half of 1% a year. Going clean
out of circulation. And then the way you throw away hundreds
of thousands of tons of phosphorus pentoxide in your sewage!
Pouring it into the sea. And you call that progress. Your modern
sewage systems!’’ His tone was witheringly scornful. ‘‘You
ought to be putting it back where it came from. On the land.’’
Lord Edward shook an admonitory finger and frowned. ‘‘On
the land, I tell you.’’ (p. 57)
A once closed-looped sustainable cycle had been opened and
phosphorus molecules now move in a linear fashion, from mines
to oceans at rates many orders of magnitudes greater than the nat-
ural biogeochemical cycle, which takes tens of millions of years.
7. From the Industrial Revolution to widespread phosphorus
pollution
With the Industrial Revolution gaining momentum, public
health concerns mandated disposal of excreta, rather than reuse.
Phosphorus was now discharged to oceans, lakes and rivers instead
of land, and thus, permanently lost from the human food system.
Cultural eutrophication of freshwaters mirrored the expansion
and development of modern industrial societies through Europe
and North America: the Wisconsin lakes – Mendota and Monona
in 1882, Lake of Zurich, Switzerland in 1896, Lake Erie in 1930
and Lake Washington in the 1950s, to name a few (Vallentyne,
1974). The most famous water-borne pollution incident being
Fig. 5. Large pile of bison skulls that will be ground into fertilizer in the US around
1870. Photograph courtesy of Burton Historical Collection, Detroit Public Library.
Fig. 6. Historical sources of phosphorus fertilizers used in agriculture globally (1800–2010). The dramatic increase in phosphate rock production in the middle of the 20th
century is indicated. Source: updated from Cordell et al (2009).
742 K. Ashley et al. / Chemosphere 84 (2011) 737–746
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‘‘The Great Stink’’ when British Parliament was disrupted in the
summer of 1858 due to the stench from the raw sewage enriched
Thames River (Fig. 7); this, no doubt, guaranteed political support
for construction of London’s new sewer system (Johnson, 2006).
The sanitary engineering community responded to the increas-
ing prevalence of water closets and emerging public health
requirements by building sewer projects (Neset et al., 2010), and
eventually developing wastewater treatment processes to stabilize
and treat human waste (Metcalf and Eddy, 1991). Elegant Victorian
schemes to pay for new sewer systems, by marketing cash crops
from ‘sewage farms’, were largely dismissed; not because the idea
was faulty, but because the early examples were flawed due to
location, wet weather, and poor management (Goddard, 1996). In
early 20th century Sweden, waste products from the emerging
‘consumer society’ (i.e., broken glass and metal tins) contaminated
household excreta, and contributed to the abandoning of returning
nutrients to farmlands (Neset et al., 2010).
The resulting problems of receiving water pollution soon inten-
sified; sanitary engineers initially addressed the problem by build-
ing longer sewers (Edmondson, 1991), and eventually developed
more sophisticated wastewater treatment processes: this included
secondary treatment, to further reduce biochemical oxygen de-
mand. The rapidly expanding economies and populations in the
post WW II western world, plus the introduction of detergent
phosphates, led to increasingly widespread eutrophication and
subsequent scientific investigations to resolve the ‘‘Great Phospho-
rus Debate’ (Vallentyne, 1974). Although numerous independent
investigations identified phosphorus as the key element in eutro-
phication (National Academy of Sciences, 1969), a single photo-
graph of an experimentally divided lake in northwestern Ontario,
Lake 226, led to bans on the use of detergent phosphates, as well
as implementation of tertiary wastewater treatment to remove
nutrients from point source effluent streams (Schindler and Vallen-
tyne, 2008; Schindler, 2009). Tertiary treatment was initially
achieved by chemical precipitation, which permanently removed
phosphorus from the human food system and created significant
waste sludge disposal problems. Later, phosphorus was removed
by the more elegant and sustainable Biological Nutrient Removal
process (Barnard, 1975), and the problem with phosphorus man-
agement appeared to be solved – or was it?
Unfortunately, waste treatment for animal manures remained
at medieval levels of sophistication, as it does to this day. This ar-
chaic situation, coupled with increasing use of fertilizers from the
‘Green Revolution’, global trends in agri-business herd densifica-
tion, biofuel farming and increasing dietary consumption of meat,
has created a global epidemic of point and non-point source eutro-
phication, with degraded water quality conditions reminiscent of
Victorian London. From the Baltic, to Canada’s Lake Winnipeg, to
New Zealand’s Rotorua lakes, Chesapeake Bay, the Gulf of Mexico
and much of China, the global footprint of eutrophication is rapidly
expanding and permanently removing phosphorus from the
world’s food system. In 1974, J.R. Vallentyne predicted that by
the year 2000 we would be living in an environmental disaster
he called the Algal Bowl: it was an accurate prediction, indeed
(Vallentyne, 1974).
8. A new era: global phosphorus scarcity
While phosphorus has largely been managed as a pollutant to
date, the 21st century is witness to a new dominant understanding
of phosphorus as a globally scarce resource. Some scientists and
philosophers have warned about future phosphate scarcity for dec-
ades – if not centuries. As early as 1798, Thomas Malthus ex-
pressed concerns that global population would eventually be
constrained by food supply (Linnér, 2003). Later echoed by Mead-
ows et al (1972) in their seminal work ‘Limits to Growth’, which
suggested that certain elements were of finite supply on planet
earth, and that one day they could be depleted. They warned that
the current trajectory of resource use could not continue indefi-
nitely and would eventually lead to collapse. With specific refer-
ence to finite phosphate rock resources and implications for
humanity, Aldous Huxley’s character Lord Howard in his 1928
novel Point Counterpoint proclaims:
‘‘you think you can make good the loss with phosphate rocks.
But what’ll you do when the deposits are exhausted?....What
then? Only two hundred years and they’ll be finished. You think
we’re being progressive because we’re living on our capital.
Phosphates, coal, petroleum, nitre - squander them all. That’s
your policy.’’ (Huxley, 1928)
Sixty years ago M. King Hubbert (1949) showed the world that
that oil production would eventually reach a peak of instantaneous
production and then decline, constrained by energy and economics
of extracting lower quality and less accessible reservoirs (Deffeyes,
2003). The critical point in time will therefore be much sooner than
when 100% of the resource is depleted. Hubbert proved this empir-
ically using production data from the US oil reservoirs. Like oil,
phosphate rock is a non-renewable resource and a critical resource
on which society currently depends. Production of phosphate rock
is estimated to peak around 2030–2040 concurrent with a rising
demand from a growing and hungry world population, trends to-
wards more meat and dairy-based diets, the need to boost soil fer-
tility in some regions and demand for biofuels and other non-food
commodities (Cordell et al., 2009). The more pessimistic analysis
by Dery and Anderson (2007) suggested peak phosphorus already
Fig. 7. Carricature of Prof. Faraday giving his business card to the odiferous Father
Thames. Source: A cartoon in Punch Magazine, July 1855, by artist John Leech.
K. Ashley et al. / Chemosphere 84 (2011) 737–746 743
Author's personal copy
occurred in 1989. However this was likely to be a mini-peak due to
the collapse of the Soviet Union and reduced demand from Europe
and North America (see Cordell et al., 2009 for further explana-
tion). The latest International Center for Soil Fertility and Agricul-
ture Development (IFDC) report suggests there are 60 000 Mt of
phosphate rock reserves, compared to previous US Geological Sur-
vey (USGS) estimates of 16 000 Mt (Van Kauwenbergh, 2010).
However, these new IFDC figures only increase the estimates for
Moroccan phosphate reserves based on a 30 year old report, are
only estimates based on ‘‘inferred’’ reserves, which have not been
verified by on-site prospecting and ore grade analysis, nor been
independently verified, hence must be viewed with considerable
caution. Further, the new reserve estimates do not remove the
threat of peak phosphorus; they only delay the peak by several
decades.
Whist there is a vigorous debate today around the lifetime of
phosphate rock reserves or the timeline of peak phosphorus, what
is clear is that the remaining rock is lower in phosphorus concen-
tration (%P
2
O
5
), higher in contaminants, and more difficult to ac-
cess, in environmentally or culturally sensitive areas; it will
require more energy to extract and produce, and will cost more
to refine and ship (Cordell et al., 2009). Further, unlike oil, phos-
phorus cannot be substituted for, when it becomes scarce or
expensive. As put eloquently by Asimov:
We may be able to substitute nuclear power for coal, and plas-
tics for wood, and yeast for meat, and friendliness for isolation -
but for phosphorus there is neither substitute nor replacement
(Asimov, 1974).
An ultimate goal of sustainable phosphorus use is ensuring that
all the world’s farmers have sufficient access to phosphorus to
grow enough food to feed the global population, whilst minimizing
adverse environmental and social impacts (Cordell, 2010).
However, already today, many poor farmers (particularly in sub-
Saharan Africa) have phosphorus-deficient soils and cannot access
fertilizer markets due to poor purchasing power. This has led not
only to low crop yields, but also increasing losses due to soil ero-
sion, poor farmer incomes and increased hunger. Indeed, many of
the world’s 1.02 billion undernourished people are smallholder
farmers (IAASTD, 2008; FAO, 2009).
Further complicating the picture, is that just five countries con-
trol 85% of the world’s remaining reserves – Morocco, China, US,
Jordan and South Africa (Jasinski, 2010). If the 2010 IFDC report
were accurate, this would mean Morocco alone controls 85% of
the world’s phosphate rock reserves. A spike in the price of food,
oil, fertilizers and other raw materials in 2008 triggered food and
farmer riots. An unprecedented 800% price spike in phosphate rock
affected the world’s farmers and led to China imposing a 135% ex-
port tariff on phosphates; this effectively halted exports from one
of the largest producing countries (Fertilizer Week, 2008). Morocco
controls the world’s largest remaining high quality phosphate re-
serves – including the portion that occurs in Western Sahara, con-
trary to UN resolutions. The US, formally the world’s largest
producer, consumer, importer and exporter of phosphate rock,
now has only decades left of it is own reserves (Cordell, 2010;
Jasinski, 2010). Whilst phosphate prices eventually dropped from
800% to only 200–300% higher than 2007 levels (partly due to
the economic crisis), this short-term crisis can be seen as a warning
of things to come. The 2010 United Nations Food Price Index now
exceeds the 2008 spike and is widely believed to be contributing to
the unprecedented political tumult in the Middle East.
While modern society has been preoccupied with concerns
about international terrorism and climate change (which are enor-
mous social and environmental problems intimately linked to
combustion of fossil fuels) the companion ‘show stopper’ of peak
phosphorus has attracted little attention, until recently. The con-
vergence of peak phosphorus, peak oil and water shortages in a cli-
matically stressed mid-21st century world is already raising
concerns among the world’s military strategists (Dyer, 2008).
9. Learning from the past: towards a sustainable phosphorus
future?
Averting a major phosphorus crisis is possible; however, it will
require considerable political will and substantial changes to our
current physical infrastructure and institutional arrangements.
While we do not need to revert back to the ways of the ‘dark ages’
and carry our own excrements in buckets to the field, we do funda-
mentally need to return to a nutrient reuse society, in order to sus-
tain our population into the future and protect the aquatic
environment. Sustaining global and local phosphorus cycles can
only be achieved through recycling close to 100% of the phospho-
rus temporarily lost from the food production and consumption
system – including human excreta, manure, food and organic
waste. Drangert et al. (2010) reflects that, while humanity was pre-
viously in an era of nutrient recycling for tens of thousands of
years, we may merely be in a brief period in history where the
phosphorus cycle has been broken and the sanitation-food link
temporarily disconnected.
Investing in renewable phosphorus sources (through local
phosphorus recovery from wastes) can simultaneously reduce
dependence on a finite resource, reduce water pollution and in-
crease communities’ phosphorus security, which is particularly
important for regions highly dependent on imports – from Europe
to sub-Saharan Africa. Today’s extremely long and globalized food
commodity chains have led to numerous points of phosphorus
losses and inefficiencies; so much so that only a fifth of the phos-
phorus mined to produce food actually reaches the food we eat
(Cordell et al., 2009). The remainder is lost (permanently or tempo-
rarily) during mining and fertilizer production, application and
harvest, livestock rearing, food processing and retail and finally
during consumption and excretion. This presents numerous oppor-
tunities for increasing efficiency of phosphorus use and reducing
unnecessary spillages, wastage and ecosystem degradation.
There is no single solution to replace the massive consumption
of phosphate rock. Sustainable measures aimed at recovering and
reusing phosphorus in the food system can range from low-tech,
small-scale solutions like direct urine reuse, through to large scale,
high-tech solutions such as struvite recovery from wastewater
treatment plants (Britton et al., 2009; Cordell et al., 2011). Solu-
tions will need to be region-specific, to ensure they are appropriate
for the local environmental, political, economic, demographic and
cultural conditions; they must also be harmonious with the re-
gion’s sanitation and food security situation.
It is particularly important that developing countries re-exam-
ine their aspirations for ‘western-style’ sewage treatment solu-
tions, and not automatically adopt the ‘water carriage central
end-of-pipe treatment’ paradigm, which is among the most expen-
sive and energy intensive components of modern public infrastruc-
ture (Abeysuriya et al., 2006). This ‘once through’ paradigm was
designed to solve the emerging disease and pollution problems
of Victorian London and other 19th century Industrial Revolution
cities; however, it is not necessarily the optimal solution for the
21st century developing world, or in the developed world as aging
infrastructure systems become due for replacement. Alternatives
such as decentralized systems, waste-stream separation at source,
and ‘improved’ centralized systems should be considered (Abey-
suriya et al., 2006); the focus should be on recovering water, heat
energy, carbon, nitrogen and especially phosphorus, to once again
‘close the circle’ and become truly sustainable.
744 K. Ashley et al. / Chemosphere 84 (2011) 737–746
Author's personal copy
Given the importance of phosphorus to our very existence, it is
perhaps surprising that there are no explicit governance structures,
such as policies or organizations, that specifically address the long-
term availability and accessibility of phosphorus for global food
security (Cordell, 2010). Thus, there is a strong need for effective
governance to ensure a coordinated response to phosphorus acces-
sibility for all farmers and looming phosphorus shortages, exacer-
bated by a global population of 6.7 billion humans, 63 billion
livestock, and now competing demands for phosphorus for non-
food purposes (such as growing biofuel crops which require ongo-
ing fertilization or lithium-ion-phosphate electric vehicle batteries
that each contain 60 kg of phosphate) (Cordell, 2010). We will need
to confront our diets, and reverse the recent global trend towards
more phosphorus-demanding meat-based diets; we should con-
sider shorter food production and consumption chains, such as ur-
ban agriculture fertilized with urban phosphorus-containing
‘waste’ streams, in order to secure a sustainable phosphorus cycle
and feed humanity in the future. The stark reality is that the eco-
logical footprint of 63 billion livestock, even at a conservative
10:1 animal to human ratio, represents a global planetary footprint
of over 630 billion humans, which is not sustainable. In addition,
the phosphorus leakage from supporting this massive agricultural
biomass is the dominant contributor to the global epidemic of non-
point source eutrophication, which is degrading the world’s fresh
waters and near-shore coastal zones at an accelerating rate (World
Resources Institute, 2008). Clearly, a ‘Fourth Revolution’ is required
to resolve this dilemma, as the ‘phosphorus footprint’ of the
world’s standing livestock dwarfs their human counterpart.
10. Conclusions
This paper has shown how the Industrial, Sanitation and Green
Revolutions have altered human use of phosphorus, shifting from
close-looped phosphorus-food systems to unsustainable linear
paths that have simultaneously lead to a global environmental
challenges of phosphorus pollution and scarcity. Increasing envi-
ronmental, economic, geopolitical and social concerns about the
short- and long-term use of phosphate rock in agriculture means
there is an urgent need to reassess the way crops obtain their phos-
phorus and humanity is fed.
Anadromous fish such as sockeye salmon (Oncorhynchus nerka)
are an interesting example of a source of phosphorus flux from the
ocean back to the terrestrial ecosystem (Stockner and Ashley,
2003). When salmon migrate upstream to spawn and die they re-
turn nutrients from the ocean, which is recycled in the aquatic
environment and a portion typically consumed by carnivores such
as bears and numerous scavengers, which is then deposited in
riparian and upland areas, thus enriching the terrestrial environ-
ment. Hopefully, we are intelligent and observant enough to learn
from nature and follow their lead towards an environmentally sus-
tainable future where phosphorus, and other limiting nutrients, are
captured and recycled ad infinitum.
A globally emerging paradigm is now in place (Abeysuriya et al.,
2006). As evidenced by nutrient recovery conferences held recently
(e.g., Ashley et al., 2009), increased technical publications and
theme articles in internationally published literature, both public
and political awareness of the ‘phosphorus issue’ is becoming more
widespread. Phosphorus recovery and reuse from domestic waste-
water is already expanding and targeted agricultural wastes, such
as dairy and hog manure, is on the horizon. With phosphorus now
becoming a ‘strategic’ commodity in the global marketplace, the
pathway ahead is very clear. The fate of humankind on this planet
may, indeed, rest on this recognition factor.
Clearly, a Fourth Revolution is required, which we will term
‘‘The Sustainable Agri-Food Revolution’’. It is widely acknowledged
that the most valuable needs of the 21st century planet, with
potentially 9 billion humans and 90 billion livestock (if the 1:10 ra-
tio remains), will be clean water and adequate nutrition. Neither of
these basic needs will be achievable, especially in the developing
countries, if we do not start now to reform the use of phosphorus
in the global agricultural-food production system. No doubt some
governments and industries will mock and oppose these ideas, just
as some have used obfuscation and denial to avoid the realities of
climate change (Hoggan, 2009). Universities and NGO’s will play a
key role in this regard, as sources of factual information and unbi-
ased policy recommendations. History has repeatedly shown that
conflicts often arise between countries over resource inequities
(Klare, 2001; Dyer, 2008), and we need not follow that path when
peaceful, and truly sustainable alternatives, are possible.
Acknowledgements
We would like to thank Dr. James Barnard, Dr. Bill Oldham, Mr.
Fred Koch and Dr. Jan-Olof Drangert for their vision and inspiration
on phosphorus recovery, and for many enjoyable conversations on
how to realistically achieve this goal.
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