Chemosphere 84 (2011) 822831

Contents lists available at ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Improved phosphorus use efciency in agriculture: A key requirement for its

sustainable use
J.J. Schrder a,, A.L. Smit a, D. Cordell b,c, A. Rosemarin b
a

Agrosystems Department, Plant Research International, Wageningen University and Research Centre, PO Box 616, 6700 AP Wageningen, The Netherlands
Stockholm Environment Institute, Krftriket 2B, SE-106 91 Stockholm, Sweden
c
Institute for Sustainable Futures, University of Technology, Sydney, PO Box 123, Broadway, NSW 2000, Australia
b

a r t i c l e

i n f o

Article history:
Received 16 September 2010
Received in revised form 25 January 2011
Accepted 31 January 2011
Available online 24 February 2011
Keywords:
Fertilizer
Land use
Manure
Phosphorus
Efciency
Surplus

a b s t r a c t
Mineral phosphorus (P) fertilizers processed from fossil reserves have enhanced food production over the
past 50 years and, hence, the welfare of billions of people. Fertilizer P has, however, not only been used to
lift the fertility level of formerly poor soils, but also allowed people to neglect the reuse of P that humans
ingest in the form of food and excrete again as faeces and urine and also in other organic wastes. Consequently, P mainly moves in a linear direction from mines to distant locations for crop production, processing and consumption, where a large fraction eventually may become either agronomically inactive due to
over-application, unsuitable for recycling due to xation, contamination or dilution, and harmful as a polluting agent of surface water. This type of P use is not sustainable because fossil phosphate rock reserves
are nite. Once the high quality phosphate rock reserves become depleted, too little P will be available for
the soils of food-producing regions that still require P supplements to facilitate efcient utilization of
resources other than P, including other nutrients. The paper shows that the amounts of P applied in agriculture could be considerably smaller by optimizing land use, improvement of fertilizer recommendations and application techniques, modied livestock diets, and adjustment of livestock densities to
available land. Such a concerted set of measures is expected to reduce the use of P in agriculture whilst
maintaining crop yields and minimizing the environmental impact of P losses. The paper also argues that
compensation of the P exported from farms should eventually be fully based on P recovered from wastes,
the recycling of which should be stimulated by policy measures.
2011 Elsevier Ltd. All rights reserved.

1. Introduction
In the pre-industrial era, processing and consumption of food
were closely connected. Wastes, if looked upon as that at all, were
recycled locally. Crop yields in these agro-ecosystems were limited
by the amounts of available nitrogen (N) and phosphorus (P).
Losses of nutrients per unit area were small and compensated by
regular ooding, weathering, atmospheric deposition, shifting cultivation, soil fertility imported via livestock grazing on surrounding
rangeland, and by biological N xation (Fig. 1). The gradual decrease of labour hours per unit yield stimulated migration to towns
where education, science and industrial production started to
ourish. Knowledge and technologies emerging from these towns
and industries helped to further expand the area under tillage
and increase yields per hectare, particularly due to manufactured
N and P fertilizers. Increased agricultural production allowed the
human population to grow and afforded humankind a more afuent diet (Brown, 2003). At this point agro-ecosystems changed
Corresponding author. Tel.: +31 317480578; fax: +31 317481047.
E-mail address: jaap.schroder@wur.nl (J.J. Schrder).
0045-6535/$ - see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.chemosphere.2011.01.065

from self-controlling systems with a negative feedback constrained

by the nutrients provided by nature, to systems with a positive
feedback in which humans themselves produced the nutrients
needed to boost food production. Moreover, manufactured fertilizers alleviated the necessity to recycle the N and P leaving farms in
the form of marketed products and allowed the segregation of
mixed farming systems and, more generally, of production, processing and consumption as such (Fig. 2). However, the drawback
of such ever-expanding systems is that they are unsustainable.
Modern agro-ecosystems deplete nite resources (land, fossil
water, fossil energy, fossil phosphate) and contaminate an ever larger part of the planet with reactive N and P to the detriment of
environmental quality including biodiversity (Correll, 1998; Erisman, 2009).
Agriculture alone results in the depletion of approximately 19
Mt a 1 of P from phosphate rock for fertilizer production (Heffer
and Prudhomme, 2008). However, due to inefciencies in the food
production and consumption chain, only one-fth of this P reaches
the food eaten by the global population (Cordell et al., 2009). The
depletion rate of reserves for P fertilizer production (and the
associated emissions of P due to the use of fertilizers, manures

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

823

Fig. 1. Phosphorus uxes in pre-industrial societies.

Fig. 2. Phosphorus uxes in industrialized societies.

and human waste), are expected to increase as the world population will grow by another 3 billion people over the next 40 years
(United Nations, 2007). Moreover, increased per capita use of fertilizer P is imminent due to a gradual change towards diets richer
in meat and dairy products for which more feed crops must be produced. Further, an additional need for fertilizer P may be triggered
by the decision to grow bio-energy crops, in particular if these
crops are to be grown on marginal land, poor in nutrients, to avoid
competition with food and feed production and if nutrients in the
associated ashes or cakes are not recycled (Lott et al., 2009; Smit
et al., 2009).
Whenever a resource is nearing depletion, people and institutions typically call for more efcient use. Efciency alone, however,
is not sufcient to manage a nite resource as long as the loss rate
is orders of magnitude greater than the geological regeneration of
new reserves. Indeed, under a business-as-usual (BAU) scenario,
the easily accessible, high grade phosphate rock reserves are likely
to be depleted within 50150 years. Further, the critical point in
time when production peaks (peak phosphorus) is predicted to
occur by 2035, after which demand will outstrip supply (Cordell
et al., 2009). While the exact timeline of the peak is somewhat dis-

puted due to poor data and the potential inuence of external supply or demand-side factors (PrudHomme, 2010; Cordell and White
(2010)), the underlying principles remain. It is widely accepted
that phosphate rock reserves are decreasing in grade (% P205 content) and accessibility, and increasing in contamination levels,
requiring additional energy inputs and costs.
Improved use efciency in agriculture (and other key stages
of the food production and consumption systems), could substantially reduce the global demand for P and, hence, postpone
the depletion of fossil reserves (Cordell et al., 2009). Such measures can essentially buy the time to develop and implement a
truly sustainable solution that involves complete recycling of P
from industries and urban areas back to agriculture. A full and
safe recycling of that P requires re-integration of our food production, processing and consumption system. The present paper
reviews current P use efciency in agriculture and identies
measures for improved efciency. Examples from the European
situation are provided. A parallel paper (Cordell et al., this issue)
compliments this by systematically examining the potential for P
recovery from industries and urban areas and its reuse in
agriculture.

824

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

Table 1
Soil surface balance of agricultural land for phosphorus (kg P ha
Balance terms:

Inputs

Mineral fertilizer
Organic
Deposition
Seeds
Total

Outputs

Harvested/grazed

Surplus

) in OECD countries in 2004 (OECD, 2010b).

Countrya
BE

NL

PT

UK

DK

IT

ES

LU

FI

EU15b

IE

EL

FR

SE

AT

PL

DE

CZ

SK

HU

18
30
0
0
48

12
33
1
0
45

7
18
0
0
25

9
13
0
0
22

8
19
0
0
28

14
17
0
0
32

9
18
0
0
27

19
16
0
0
35

9
8
0
0
17

9
12
0
0
21

10
15
0
0
25

5
6
0
0
12

11
11
0
1
22

6
8
0
0
14

6
10
1
0
17

8
7
0
1
15

9
14
0
0
23

6
6
1
0
13

3
5
0
0
8

6
5
0
0
11

28

29

17

22

18

26

10

17

19

20

12

15

14

23

14

10

15

21

16

15

13

11

10

BE Belgium, NL Netherlands, PT Portugal, UK United Kingdom, DK Denmark, IT Italy, ES Spain, LU Luxemburg, FI Finland, IE Ireland, EL Greece, FR France, SE Sweden, AT
Austria, PL Poland, DE Germany, CZ Czech Republic, SL Slovakia, HU Hungary.
b
Mean weighted for the areas per country.

2. P surpluses and use efciency in agriculture

Use efciency in any conversion process, is commonly assessed
by comparing the amounts going out in as far as these are appreciated (output) to what has gone in (input). The difference between both, the surplus, is in general deemed to be lost. If more
P is applied to a eld than removed in harvested crop material,
then there is a positive soil surplus. However, great caution is required when using these surpluses as a proxy for losses. First of
all, the discrepancy between inputs and outputs can only be accurately determined if all the relevant input and output terms are included. For example, the true output of a eld of cereals is
generally not the amount of P taken up by the whole crop (grain,
stalk, leaves, stubble, roots) but just the P in grain, provided the
crop residues are returned to the soil. Moreover, a positive surplus
of the common balance set-up is not necessarily indicative of the P
lost to streams, lakes and oceans, as P is relatively immobile in soils
due to various chemical reactions (Laegreid et al., 1999; Hilton
et al., 2010). A negative balance outcome is at the same time not
a guarantee for the absence of P losses, because dissolved or particulate P can have left the soil pool through leaching or run-off. For
exactly the same reason the use of ratios (P output/P input) as indicator of use efciency, also deserves caution (Schrder et al., 2003).
According to OECD denitions the input variables of the P soil
surplus balance consist of (1) mineral fertilizer P, (2) P in manure
and other organic amendments, (3) atmospherically deposited P,
and (4) P in seeds. Outputs are the P in harvested crops and grazed
vegetation (OECD, 2010a). Estimating all these variables is aficted
with errors to a greater or lesser extent. The relative error for the
input variable mineral fertilizer is low because of its relatively
accurate registration and constant composition. The same holds
true for the impacts of errors related to deposition and seeds as
these two items generally contribute less than 1 kg P ha 1 a 1.
The manure input variable, however, is associated with a larger potential error because OECD deduces it from livestock numbers and
national default values for the P excretion per animal category, the
latter values not always being plausible (Schrder et al., 2010). Errors associated with the output variables can also be considerable.
This is not only so because the amounts of P removed are based on
national default values instead of actual values for P concentrations
per crop type, but particularly because the yields of grazed crops
are based on estimates that have at best been approximated from
the observed livestock production and attending feed requirements (OECD, 2010a). Despite these uncertainties, P soil surpluses
give at least an approximation of the use efciency of P in current
agricultural production systems.
The collection and processing of these data is time consuming.
Consequently, the most recent overview of P soil surpluses in individual European countries, as provided by OECD, pertains to 2004
(OECD, 2010b). As for the 15 member states comprising the

European Union (EU) in 2004 (EU15), the surplus per unit area of
agricultural land ranges from values close to zero in Eastern Europe
to 20 kg P ha 1 in parts of Western Europe. The surplus averages
5 kg P ha 1, which is close to the 8 kg P ha 1 that Richards and
Dawson (2008) estimated in the year 2006 for the present EU27
as a whole. The differences between countries are considerable
(Table 1). As livestock densities in Europe have hardly changed
since 2004 (Eurostat, 2010a) it is not likely that the manure input
term of the P balance has changed very much. It is also unlikely
that the inputs of P via deposition or seeds and the outputs of P
via harvests have signicantly changed in the course of time. The
input of mineral fertilizer has changed only slightly. According to
EFMA data (Eurostat, 2010b) mineral fertilizer use decreased by
0.2 kg P ha 1 a 1 between 1999 and 2008 in Western Europe,
whereas the use increased by on average 0.2 kg P ha 1 a 1 during
this period in Eastern Europe. These developments allow us to conclude that present P surpluses (2010) will probably differ less than
a few kg P ha 1 (in either direction) from the 2004 OECD surpluses.
The signicant magnitude of the European P soil surpluses (up to
approximately 20 kg P ha 1 a 1 in individual member states) indicates a large scope for developing and implementing measures to
improve the use efciency.
3. Potential measures to improve the P use efciency in
agriculture
This section reviews a range of potential measures to improve P
use efciency. Both the nature of current inefciencies and opportunities for improvement are identied and discussed. The analysis
starts with agricultural land use as such and the losses to which
tilled soils in particular are exposed. Subsequently, we take a closer
look at the P ows crossing the boundaries of an individual eld.
Finally, we expand this system with a livestock component and
the attending measures needed for a better P use efciency in
farms that involve both crops and animals.
3.1. Optimising land use
Agriculture is mainly an outdoor activity and growing conditions are thus not always fully under control. Consequently, some
losses of P are probably inevitable even if soils, crops and fertilizers
are managed according to the best available techniques. On a global scale these inevitable losses from elds will be more extensive,
the larger the area under agriculture and the higher the P content
of the soil. It is therefore imperative to nd the optimal balance between a sufciently high productivity per hectare, limiting land demand but requiring a sufcient P content, and keeping P contents
in soils low as to minimize losses per hectare, albeit it will require
more land to produce the same volume of food on P decient soils.

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

Whatever the position on this balance, the composition of the human diet is also a determinant of land use and attending P losses,
since more land is generally needed to produce meat and dairy
products than vegetal-based products (Gerben-Leenes and Nonhebel, 2002). The same holds for additional land claims to produce
bio-energy crops (Smit et al., 2009).
3.2. Preventing erosion
P is not only depleted from soils by growing crops but also due
to erosion. Erosion encompasses water erosion, wind erosion, tillage erosion and the erosion resulting from soil particles adhering
to lifted crops such as sugar beets (Verheijen et al., 2009). Louwagie et al. (2009) reported that of the total European land area 12%
suffers from water erosion and 4% from wind erosion. Water erosion is above all a problem in Southern Spain, Western Italy and
Greece and is determined by the slope gradient, the slope length,
rainfall and rainfall distribution. Wind erosion is mainly an issue
in a belt of sandy soils stretching from the south of England via
The Netherlands, Denmark and Northern Germany to Poland. Both
types of erosion predominantly occur in tilled elds, in particular
when crops leave the soil uncovered for a longer period. Examples
of such crops include potatoes, sugar beets, maize, and sunower
(Louwagie et al., 2009).
Quantifying the P loss associated with erosion is fraught with
difculty. Firstly, eroded material is not really lost as long as it is
deposited and subsequently accounted for as an input in the
receiving agricultural area. Secondly, quantication is also troublesome because data sets tend to be derived from experiments in regions where erosion is an issue. Up-scaling these data to a larger
area including the more at regions in particular those with a permanent cover in the form of grassland, is an inaccurate process.
Estimates of the amounts of soil lost via erosion range from 5 to
40 Mg ha 1 a 1 for an average European arable soil (Verheijen
et al., 2009) to 10 Mg ha 1 a 1 at most for the major part of Europe
(Louwagie et al., 2009). Thirdly, it is even more complicated to
translate these losses of soil into P losses as that requires knowledge of the P-concentration in the eroded material. A limited
amount of material can be associated with a high P loss, as the light
and more easily erodible soil fraction (clay) tends to contain more
P than the coarse fraction (Quinton, 2002). Data provided in Hooda
et al. (2000) suggest that P-concentrations in an average European
soil range between 0.05% and 0.10%. This implies that erosion of
10 Mg of soil ha 1 a 1 represents an annual loss of 510 kg P
ha 1. This is a considerable amount but less than the numbers given in Smil (2000) and Ruttenberg (2003) who estimate that at a
global scale 2030 Mt a 1 of P is lost via erosion. This would be
equivalent to an annual loss of 1520 kg P ha 1, assuming that erosion from land other than arable land is negligible. More recently
Liu et al. (2008) provided data suggesting that approximately 13,
8 and 3 kg P ha 1 is annually lost from arable soils, overgrazed pastures and ordinary pastures, respectively.
Regardless of the exact quantity of P lost, the magnitude of the
loss justies measures. If eutrophication starts from a P concentration in water of around 0.10 g total P m 3 (Correll, 1998), no more
than 0.20.6 kg P ha 1 should be eroded by a typical European precipitation surplus of 200600 mm, to keep surface water from
eutrophying. Many of the erosion abatement measures are hence
directed at improving the inltration capacity of soils, such as:
minimum tillage without removal of crops residues (mulching),
ridge tillage, sub-soiling, terracing, contour ploughing, buffer stripping, cover crop establishment, conversion of arable land into
grassland, agro-forestry, or complete reforestation (Louwagie
et al., 2009). Uri and Lewis (1998) reported that this type of measures were able to reduce erosion loss in the United States by 42%
between 1982 and 1997. Deasy et al. (2010) recently evaluated

825

mitigation options for P loss from winter cereals in the United

Kingdom. They concluded that disturbing the soil in xed wheel
tracks (tramlines) with a tine, in particular, reduces erosion-related P loss by up to 99%. Common European bans on the spreading
of fertilizers and manures on frozen or snow-covered land (De
Clercq et al., 2001), combined or not with a mandatory incorporation, also reduce the risk of erosion and P loss, including the loss
that may also occur via the less visible process of surface run-off
from seemingly at but water-logged elds.
Erosion brings about the need for additional P inputs if the fertility of soils is to be maintained, but might eventually also lead to
their complete abandonment. This may in turn result in reclamation of new areas that often need large P inputs before becoming
productive at all. Generally, statistics on net land use do not reveal
this turnover rate due to soil degradation, let alone its implication
for P demand.
3.3. Maintaining soil quality
The presence of P in a soil is not a guarantee for its productiveness. Soils must full many other characteristics to assure that this
P is available to crops and that it can be efciently utilized, once
taken up. This complex set of characteristics is called soil quality
(Beare et al., 1999). It encompasses aspects such as having the right
pH, organic matter content, resilience against physical and biological perturbations, and fertility enhancing biodiversity. However,
too much focus on each of these aspects in isolation and beyond
reason (Loveland and Webb, 2003), can harm rather than improve
the use efciency of resources. Returning crop residues to the soil,
for instance, may stimulate soil life and thus improve soil structure, but implies that these residues are no longer available as feed
or fuel. The concept of soil quality is therefore still a subject of
erce debates (e.g. Giller et al., 1997; Letey et al., 2003). Regardless
of this ongoing debate, it is absolutely safe to say that more P will
be needed to attain a certain yield if the pH of a soil is suboptimal,
if soils contain too little or too much water, or if soil compaction
hampers root growth. Optimising the structural soil quality can
thus increase the accessibility of P reserves in deeper soil layers, reduce the need for fertilizer P supplements, and improve the use
efciency of P. Johnston and Dawson (2010) proved that it is indeed the organic matter mediated soil structure rather than the organic matter itself that improves the availability of phosphorus. A
60% increase of the organic matter content (i.e. from 1.5% to 2.4%)
reduced the Olsen P value required for near maximum yields in
their Rothamsted trials from, on average, 46 to 17 mg kg 1 under
eld conditions, whereas this apparent effect of organic matter
did not occur in a pot experiment once these soils were sieved
and lost their structure.
3.4. Improving fertilizer recommendations
Plants will not grow if their roots cannot nd P in the soil (Laegreid et al., 1999). Yields on about two-thirds of the global farmland are limited by insufcient soil P levels (Cakmak, 2002).
Hence, most farmers apply P in the form of manures, composts,
bio-solids or mineral fertilizer, just alone to compensate for the P
that is exported in produce (that is in crops, meat, eggs, milk, wool,
etc.). In Western Europe generally more P is added than exported
from farms. This practice is to some extent based on unjustied
fears for yield penalties but may also be based on sound economic
considerations (Neeteson et al., 2006). Crop yields are maximized if
the soil P status is high, in particular those of shallow rooting species grown in rows. As the concentration of dissolved P in the soil
water is low (Hilton et al., 2010), relatively little P is acquired via
water that plants take up for their transpiration. This implies that
crops must capture most of their P via interception, that is via

826

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

growing roots scavenging the surrounding soil volume (Hilton

et al., 2010). Annual crops can be short of P, especially at a young
stage. The daily uptake of P in kg per ha may be low then, but
the daily uptake demand per unit of root length is relatively high,
as the root proliferation is just starting (Fig. 3). Under these circumstances only a high P status will facilitate a sufcient diffusion
of P to the root surface. Unfortunately, large amounts of P are
needed to improve the P status compared to the annual off-take
rate of P. This means that even farmers strictly following guidelines
for P-fertilization, must accumulate considerable amounts of P to
reach the required status. Rmer (2009) concluded that 7080%
of the soils in European countries show an average or high level
P-status. He stated that at these locations it would be possible to
maintain yields for several years even without P-fertilisation. In
Germany, as in most other European countries, a recommended
range of soil fertility applies. Rmer (2009) concluded that within
this recommended range, approximately 500 kg P ha 1 would be
needed to bring the soil from the lowest to the highest recommended fertility level. This amount is equivalent with the P taken
off by crops in around 20 years. He suggested a critical revision of
the recommendation system to ensure a more efcient use of Pfertilizer. In line with this observation, Neyroud and Lischer
(2003) and Jordan-Meille (2009) concluded that the soil tests used
for the assessment of available P in soils across Europe are anything but uniform and appear to give different recommendations
for the same soil and crop types. Climatic differences cannot always justify the observed discrepancies and this suggests that
some recommendations have been tainted by a better safe than
sorry attitude.
The match between demand and supply can be strongly improved by positioning mineral fertilizers close to the expanding
root system (starters) (Stone, 2000a,b; Ma and Kalb, 2006). The
utilization of P in manures can also benet from such a positioning
close to the anticipated crop row (Sawyer et al., 1991; Schrder
et al., 1997). In more general terms one could say that P utilization
can be improved if uniform blanket dressings would be replaced by
differentiated applications, tuned to specic needs of individual
crops and elds, of patches within elds, of particular positions
within the bulk soil, and of periods within seasons. Farming practices characterized by xed insurance shots of P, should hence be
replaced by more reasoned precision farming applications of P.
There is an obvious need for a correct assessment of the true P
requirement of soils and a better knowledge of the P-supplying
ability of the various types of inputs. As for the true P requirement

P uptake, mg km1
degree day-1

root length,
km ha-1
150 000

50
45

120 000

40
35

90 000

30
25

of soils, P should not be applied on a routine basis but instead be

determined by the amounts of plant-available P. These amounts
depend on earlier inputs and exports in crop produce and on the
tendency of some soils, for example those rich in iron or aluminium, to x P.
In relation to the ability of inputs to supply P, there is often a
misleading perception among farmers that P from a purchased
bag of mineral fertilizer is more available to crops than P from organic resources such as manures and other residues. This attitude
promotes the use of mineral fertilizer P supplements. For a long
time, the availability of P from both mineral fertilizers and organic
resources has been assessed following the so-called difference
method. This method, according to which the P uptake of a fertilized crop is compared with the P uptake of an unfertilized control,
often shows that less than 25% of the input is recovered in additional P uptake, suggesting that the remainder is not available (Hilton et al., 2010). However, this method fails to appreciate the socalled residual effect due to which the long-term availability
resulting from regular applications is close to 100% for mineral fertilizer P and P from other sources alike (Sinclair et al., 1993; Syers
et al., 2008). The truly inevitable P loss is therefore relatively low,
unless soils are rich in iron and aluminium. Inevitable P losses can
also be high if growers want to maintain the P concentration in the
bulk soil at an unnecessarily high level, like keeping a colander
lled up with water up to its brim (Hilton et al., 2010).
3.5. Fertilizer placement methods
As indicated earlier, P should preferably be applied in the most
intensely rooted parts of a soil. According to fertilizer recommendations in The Netherlands, twice as much P is needed for a similar
yield response if the fertilizer is broadcast instead of sub-surface
positioned close to seed row (Van Dijk, 2003). It is the combination
of the application method of P containing inputs and the subsequent tillage that determines whether supply and demand spatially match. This has implications for the optimal positioning of
inputs in both the vertical and horizontal plane. As far as the vertical aspect is concerned, the positioning of manure may be too
deep for a good utilization of P in an attempt to reduce the volatilization losses of ammonia-N from manure (Schrder, 2005). Shallow incorporation generally seems the right compromise, if alone
because P itself may be lost by run-off if left on top of a water-saturated soil. As for the horizontal aspect of placement, proper attention must be given to spreading techniques. Irregular, patchy
spreading patterns increase the heterogeneity of the soil fertility.
Consequently, some parts of the eld may become over-fertilised,
whereas other parts may become decient. Note that grazing
may conict with this recommendation as P rates via animal droppings will become too high in places. Such a local concentration of
P may be increased where animals tend to cluster in search of shelter or water. The previous warning for a too patchy distribution of
manure must not be seen as a general argument for a uniform distribution. In crops with a wide row distance, for instance, yields
and P utilization may benet from techniques that apply manure
close to the anticipated position of rows (Schrder et al., 1997).

60 000

20

3.6. Improving crop genotypes and promoting mycorrhizas

15
30 000

10
5
0
0

200

400

600

800

1000

0 000
1200

temperature sum, degree days, > 8 oC

Fig. 3. The summed root length of a maize crop (h) and the P uptake requirement
per unit root length (d) in the course of the growing season (expressed as degreedays above 8 C) (after Schrder, 1999).

At a young stage root length can be the limiting factor for the
acquisition of soil P. Genotypic differences in terms of the way a
plant allocates its assimilates to either aboveground parts or roots,
and differences in specic root length (root length per unit root
weight), branching or in the distribution of a given length of roots
through the soil prole, may hence affect the ability of plants to absorb P (De Willigen and Van Noordwijk, 1987). Consequently, the
required supply of soil P needed to yield a certain P uptake, and

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

consequent P uptake efciency, could be different. Lack of sufcient P uptake capacity seems to play a much smaller role in perennials of which roots exploit the total soil volume more or less
permanently. Perennial instead of annual wheat could thus represent a promising avenue (Scheinost et al., 2001). P use efciency of
crops is, however, not just determined by the uptake efciency but
also by the utilization inside the plant once the P is taken up. There
is little benet in a better uptake efciency if production of the
economically relevant plant parts per unit P taken up is lower, as
production per unit P applied would then not be improved. It is difcult to say a priori whether there is sufcient genotypic variation
of both traits (separately but, more importantly, also in their combination (Parentoni and Lopes de Souza, 2008)) to justify breeding
programs explicitly directed at the improvement of P use efciency. Decisions on investments in breeding research should consider the value for money that is to be gained via alternative
investments, that is on adjusted soil and crop management. Simic
et al. (2009), for instance, found that genotype x P fertilizer interactions of maize inbred lines were only signicant if the pH level of
a soil had dropped to an extremely low value. Liming may thus be
more cost-effective than a breeding program.
Crops can also extend their uptake capacity through a symbiosis
with benecial fungi. Associations between crops and these socalled arbuscular mycorrhizal (AM) fungi can thus improve the
availability of soil P (Bittman et al., 2006). Grant et al. (2005) attribute this to an effectively enlarged root system rather than to an
enhanced solubility of P by the fungi. Their review shows, however,
that carbon costs are involved in hosting AM fungi. Crops manage
to suppress AM fungi when the association does not pay off due to
a high P soil status. Even when the soil P status is low, the composition of the crop rotation and tillage practices do not always support a sufcient presence of AM fungi. This may require adoption of
minimum tillage techniques, seed inoculation or adjustments of
the crop rotation (Grant et al., 2005).
The use of LPA mutants (cereals with a lower content of phytic
acid) for food and animal feed, may be another promising avenue.
Lott et al. (2009) conclude that a widespread use of these mutants
could lead to considerable reductions in global P fertilizer
requirements.
3.7. Adjusting inputs to outputs
In the preceding sections the focus was on P inputs and their
availability to crops. Obviously, P surplus and use efciency are
also determined by the P output. The amount of P that eventually
leaves the farm via the gate may be easily overestimated. The P export from dairy farms (including exported animals), for instance,
amounts to approximately 1.2 kg P Mg of milk (Beukeboom,
1996), implying that a dairy farm producing 10 Mg milk ha 1, on
average, need an annual compensation via fertilizers or concentrates of only 12 kg P ha 1. Note that grasslands of dairy farms
may take up 45 kg P ha 1 or more but that this demand can largely
be provided by the internally re-circulated manure. In non-livestock farms the P export with crops amounts to 3 and 7 kg P per
Mg fresh weight for cereals and rape, respectively, and to approximately 0.4 kg P per Mg for sugar beet, potatoes and vegetables
(Beukeboom, 1996; Ehlert et al., 2006). Consequently, the annual
compensation needed for this export is around 25 kg P ha 1 for a
typical arable farm and less than 15 kg P ha 1 for horticultural
farms (Neeteson et al., 2006).
Circumstantial evidence for a structural overestimation of the
amounts of P exported in produce and an underestimation of the
amounts of P available from the various types of inputs, is reected
by the ongoing increase of the P status of many soils in Western
Europe (Tunney et al., 1997; Rmer, 2009; Reijneveld et al.,
2010). This suggests that P inputs can be reduced and much better

827

balanced with outputs. The over-applying of P may also stem from

the protability to dump P-containing residues (e.g. manure) on
nearby elds instead of returning them to the remote elds where
these residues originated from (see subsequent section).
3.8. Exporting manure
Any P export justies P inputs. P can leave the farm in the form
of crops, milk, eggs, meat and wool, but also in the form of manure.
As a matter of fact this has become common practice in many parts
of Europe where formerly mixed farms have been split up into
farms specialised in either crop production or landless livestock
production (Fealy and Schrder, 2008). From a purely theoretical
P use efciency point of view, it does not matter whether livestock
are fed home-produced feeds or imported feeds as long as the P
that is not retained in marketable products, that is the P in manure,
returns to the land where the feed originates from. The positive
relationship between regional livestock densities and P soil surpluses (as observed in e.g. The Netherlands, Flanders, Brittany, Po
Valley (De Clercq et al., 2001)) shows, however, that in reality such
a perfect recycling is complicated by economic and energetic considerations (Fealy and Schrder, 2008). Consequently, soils generally accumulate P in regions with a high livestock density,
whereas soils may become P depleted in regions where the feed
originates from, unless the latter are supplemented with mineral
fertilizer P. A more even distribution of livestock over the area
where the feed is produced could thus contribute to a more efcient use of P. Note that even in a mixed farm such an even distribution is often difcult as nearby elds tend to receive more
manure than remote elds, and hence more P (Vanlauwe et al.,
2007).
In regions with manure surpluses there may be incentives to
over-apply manure-P even on stockless farms. Horticultural farms,
for instance, are inclined to cover their need for organic matter
(OM) and N with free excess manure from neighbouring livestock
farms. Due to the relatively low N to P ratio and OM to P ratio, this
may easily lead to P accumulation (Schrder, 2005). This can only
be avoided by complementing rotations with crops supplying OM
and N such as cereals or legumes, notwithstanding their lower
protability. Farms in need of N rather than P could still use manures without the risk of P accumulation, if they were only to use
the liquid fraction resulting from manure slurry separation. The
associated solid fraction, rich in P, is less bulky and can thus be
more easily exported to remote farms in need of P (Birkmose,
2009; Schrder and Verloop, 2010).
3.9. Adjusting livestock diets
The previous section argued that reducing livestock numbers to
the locally available land is one of the measures to better balance P
inputs with P outputs. Reducing P excretion per animal can have a
similar result. The limitations and opportunities are addressed in
the present section.
The ability of mammals, non-ruminants in particular, to absorb
P from feed is limited. To avoid production losses due to temporary
P deciencies, livestock farmers in industrialized countries therefore select feed stocks with naturally high P concentrations or even
add P salts to feed stuffs. Globally, 5% of P demand is for feed additives, that is approximately 1 Mt a 1 of P. In the EU27, however, a
much larger share is used in feed. The EU27 imports 0.3 Mt a 1 of P
as feed additive, next to 1.6 Mt a 1 of P imported as raw material
for fertilizer production (rock phosphate, phosphoric acid) or as
commercial fertilizer (Richards and Dawson, 2008). This increased
P input via feed additives reduces the relative utilization of P within the animal and results in more manure P being produced. This
can lead to an undesired local P soil surplus. The production of

828

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

manure P can not only be reduced by reducing livestock numbers

but, what may be economically more attractive, also by reducing
the amounts of manure-P excreted per unit milk or meat produced.
P excretion can, for instance, be reduced by supplying less feed-P
the older the animal gets (so-called phase feeding), by tuning
the daily ration of individual animals to their actual production level, and by the use of articial enzymes (phytases). Such enzymes
can improve the availability of feed-P (phytate). Dietary adjustments such as these can reduce the throughput of P in farms and
can, hence, increase the utilization of P (Pfeffer et al., 2005; Kies
et al., 2006; Steen, 2006; Anah et al., 2010).
4. Discussion
4.1. Efcient is not per se clean
Efcient use of nutrients is easily misinterpreted as clean or
sustainable. However, the local loss of a nutrient in kilograms is
not just determined by inefcient use but by the mathematical product of hectares, the nutrient inputs per hectare, and the inefciency
of their use (that is: loss = hectares  (input/hectare)  (1 (output/
hectare)/(input/hectare))). So, the impact of losses can still be substantial if a high efciency is associated with a high input level or
many agricultural hectares relative to non-agricultural land use.
It is difcult to judge whether European production systems
should be extensied or intensied. From the perspective of resource use efciency (land, water, labour, energy) and wildlife conservation, intensication seems the way forward. However, from
the perspective of local environmental quality requirements,
including farmland biodiversity and wholeness, there is need for
extensication, which is probably more true in Western Europe
than in Eastern Europe. Additional research is needed to support
decisions on the optimal position on this axis in view of P use efciency (Schrder and Bos, 2008).
Attention is needed for externalizations when evaluating alternative systems. By a partial externalization of preceding or subsequent farm processes, that is by reducing the system boundaries,
the remaining system may appear to have augmented its efciency
(Schrder et al., 2003). A landless livestock farm, for instance,
exporting all its manure may seem very efcient as it will, theoretically, only lose some gaseous N. Similarly, a stockless arable farm
using no more P mineral fertilizer than the amount of P exported in
produce also has a high efciency. N and P losses and hence the
inefciencies associated with preceding processes (e.g. fertilizer
manufacturing, feed production) or subsequent processes (e.g.
recycling of manure, processing and consumption of food and feed)
are obscured by the administrative disruption of systems into subsystems (Fig. 2), in contrast to what the situation was like in preindustrial times (Fig. 1).
The P exported from farms via processing industries, markets
and our bodies, to our urine and faeces, does only partly return
to agriculture (Evans, 2008; Richards and Dawson, 2008). So even
if inputs at the farm level were accurately tuned to outputs, the
use of P is still unsustainable as long as it involves permanent reliance on rock-based mineral P instead of recycled P. Cordell et al.
(this issue) analyse the technical and cultural considerations that
currently prohibit the recycling of P containing industrial and urban wastes. They also draft the challenges and prerequisites of
handling systems that can turn these wastes into marketable P fertilizer alternatives.
4.2. Is organic agriculture the answer?
If sustainable use of P requires a better adjustment of inputs to
outputs, care for and maintenance of the soil quality, a full recy-

cling of nutrients from industries and urban areas, and minimizing

the use of nite resources such as phosphate rock, is organic agriculture then not the logical answer? After all, these are precisely
the things that the organic farming movement is advocating
(IFOAM, 2010). Before trying to determine to what extent organic
farming can indeed deliver sustainability in principle, it is informative to examine current shortfalls of organic agriculture in practice
in order to illustrate the complexity of the problem. The inputs of P
in organic agriculture may be generally lower than in conventional
agriculture, but often just as out of balance with outputs as in conventional agriculture (Watson et al., 2002). Inputs exceed outputs,
for instance, if yields and thus P outputs are limited by the frequent
lack of N in organic farming systems (Stockdale et al., 2001, 2002).
This lack of N can result from insufcient biological N xation and/
or the advocated use of solid manures which have an inherently
low N to P ratio. The European application threshold for organic
farms of 170 kg manure-N ha 1 a 1 (EU, 2008) is thus associated
with much more P than the amounts of P taken up by most crops
(Schrder, 2005). Applying these permitted rates will thus generally lead to P accumulation in soils.
The P exported in organic produce to industries and urban areas
does generally not return to organic farms, because it is still too
complicated to keep organic waste ows separated from conventional ows making them unsuitable as a certied organic input.
Further, fertilizers based on human excreta or wastewater are currently excluded from the list of permitted fertilizers in organic
agriculture standards or guidelines in many regions, including Europe (EU, 2007), India (Department of Commerce, 2005) and Australia (Organic Federation of Australia, 2005), due to the perception of
the potential heavy metal or pathogenic content. Instead, the P
outputs from organic farms may be compensated with permitted
fertilizer inputs derived from crushed phosphate rock, P imported
in organic livestock feed, or manures from neighbouring extensive
farms that, for that matter, do not necessarily need to be organic in
some EU member states. And even if the farms exporting manures
are organic, this export would yet deplete P soil fertility that may
have been built-up in a conventional past before the conversion.
A proper balancing of P inputs and outputs has also become more
difcult now that globalization has affected organic agriculture
too. The attending trans-regional ows of goods have complicated
the intended local integration of production, processing and consumption and this has limited an ideal recycling of nutrients.
As for the more theoretical considerations, it is worth noting
that the loss of P is to a limited extent an inevitable by-product
of agricultural land use as such. At least 25% more land is needed
to produce a certain diet via perfectly managed organic agriculture
than via perfectly managed conventional agriculture (Stockdale
et al., 2001). This is due to the less intensive control of pests and
diseases, lack of sufcient N or the extra land needed to grow sufcient N-xing leguminous green manures. So, from this point of
view the overall use efciency of P inputs (regardless whether
these inputs derive from rock P or recycled wastes) may be slightly
lower in a balanced organic agro-ecosystem than in a conventional
one.
While organic agriculture encourages livestock to range freely
rather than being conned indoors with little of no movement, a
trade-off from a P use efciency perspective is that the unevenly
and supercially deposited manure-P excreted outdoors may be
exposed to a larger risk of losses than the P collected from conned
animals which can be evenly applied under appropriate conditions.
This also is an argument to the detriment of organic agriculture as
far as P use efciency is concerned.
Now, if ideotypical forms of organic agriculture have this greater potential P loss as stated here, why then have its predecessors
been able to feed human populations for so many centuries? The
reason is that in the past losses of P have been compensated by

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

small but constant inputs of P through weathering, atmospheric

deposition and ooding, as well as the P brought home by livestock
that was allowed to graze on range land during daytime hours. This
system with inherent low yields could sustain itself within the
boundaries of a limited human population size and modest dietary
aspirations. Mineral fertilizers disrupted this delicate balance as
they allowed the population to grow, to adopt a more afuent diet,
and to disconnect P ows that used to replenish the P reserves of
arable land (Brown, 2003).
Some of the principles of organic agriculture could and should
nevertheless be a beacon for the use of P in any system that intends
to become sustainable. However, a smart combination of these
principles with external inputs such as environment-friendly technology and agro-chemicals may be required, unless we are prepared to feed fewer people a much more sober diet or sacrice
more wildernesses. Such smart combinations will hence yield production systems that are not literally organic, but yet provide a
sustainable use of P.
4.3. How to promote use efciency?
Several of the measures advocated in this paper can probably
pay for themselves. Lack of adoption may merely stem from lack
of awareness. Hence, information and knowledge transfer, maybe
combined with a few temporary incentives, address this part of
the problem. Measures pertaining to the adjustment of inputs to
outputs (Section 3.7), improvement of fertilizer recommendations
and application methods (Sections 3.4 and 3.5), and the adjustment of livestock diets (Section 3.9) probably belong to this group
of low hanging fruit. However, the development of new genotypes
(Section 3.6), the obliged export of manure (Section 3.8), and
investments in erosion control and the maintenance of soil quality
(Sections 3.2 and 3.3) will be more costly. This could be even more
so for interventions in land use (Section 3.1). After all, in many
cases there is a nancial rationale behind the unsustainable use
of P, as its use is associated with typical externalities, that is with
actual or potential (future) costs imposed on parties for which the
user is as yet not charged by an effective market. The costs associated with these negative effects should be internalized to make
sure that the one who decreases the opportunities of others pays
for it. If, for instance, water quality is the lost opportunity and agricultural land use is the trigger of that with P inputs, P surplus, P soil
status, P emission and P concentration acting as the intermediate
links between trigger and response, there are numerous points of
application to internalize the costs and to improve the use efciency of P. If emission is the problem, it seems preferable to
choose a parameter that is indicative of that very aspect. However,
indicators do not just need to be effective, they must also be efcient (value to be determined at low costs relative to the accuracy
of the measurement), attributable (addressing the one causing the
emission), responsive (quickly reecting changed behaviour) and
integrative (simultaneously encompassing various societal goals
to reduce the costs and administrative burdens) all at the same
time. It seems utopian to identify such an indicator, so there is
no ideal point of application for economic instruments. Handy
and simple indicators are generally not the most effective,
let alone fair indicators (Schrder et al., 2004). The P concentration
of water in a stream, for instance, is certainly indicative of water
pollution. However, measuring it can be relatively costly and does
respond very slowly to changed management. Besides, it is extremely difcult to attribute excessive values to the land users who
are to be held most responsible for the pollution. Conversely, livestock density can be easily assessed at low costs and is attributable,
but is at the same time anything but a rened predictor of losses to
water. So, additional indicators somewhere in between livestock
density and P concentration in water are apparently needed.

829

If all inputs regardless of their origin would be taxed to discourage excessive use, it would deny that inputs originating from recycled wastes are to be supported rather than charged. Moreover,
the potential loss of P is determined by the discrepancy between
inputs and outputs, that is the surplus, rather than by just inputs.
There is little point, however, in a low P surplus per unit area if the
price paid for that would be an extended demand for land to produce a required volume of crops. From that perspective it would be
better to stimulate and reward production systems with a low surplus per unit output, that is a high use efciency (surplus/output = (1/(output/input) 1)).
When designing economic instruments, due attention should
also be given to unwanted side effects. A unilateral tax on just mineral fertilizer P, for instance, could make livestock farmers decide
to compensate for that by importing more concentrates rich in P
(Fig. 2). This could offset the global merit of such a tax, particularly
if the production of these concentrates would be based on crops
that were grown abroad with untaxed mineral fertilizer P. However, if a tax on mineral fertilizer P would make arable farmers substitute excess manure from neighbouring livestock farmers for
mineral fertilizer P, taxing could certainly contribute to better balanced regional inputs and outputs of P, unless the excess manure
would be industrially processed anyhow into mineral fertilizer P.
The above examples illustrate the complexity of the issue. If the
ultimate aim is to promote recycling, to reduce the surplus per unit
area, to improve the use efciency, and discourage the excessive
use of P in general, economic instruments should probably be
simultaneously directed at different criteria.
5. Conclusion
Agricultural land loses P via erosion and exported farm products. Without compensation this will sooner or later have a negative impact on food production. Compensation is to a largely
carried out with nite phosphate rock-based mineral fertilizer P,
rather than with P recovered from wastes produced either within
the farm or downstream. This paper argues that the amounts
needed for compensation could and should, regardless the source,
be much smaller because the available measures and techniques
for a better use efciency are as yet not fully exploited.
References
Anah, S., Yazid, A.M., Anis Shobririn, M.H., Shuhaimi, M., 2010. Phytase:
application in food industry: review article. Int. Food Res. J. 17, 1321.
Beare, M.H., Williams, P.H., Cameron, K.C., 1999. On-farm monitoring of soil quality
for sustainable crop production. In: Proceedings of the 1999 Fertilizer and Lime
Research Centre Conference, Massey University, Palmerston North, New
Zealand, pp. 8190.
Beukeboom, J.A., 1996. Forfaitaire gehalten voor de mineralenboekhouding.
Informatie-en Kennis Centrum Landbouw, Ede, The Netherlands, 22 pp (in
Dutch).
Birkmose, T.S., 2009. Nitrogen recovery from organic manures: improved slurry
application techniques and treatment: the Danish scenario. In: Proceedings 656.
International Fertiliser Society, York, UK, pp. 124.
Bittman, S., Kowalenko, C.G., Hunt, D.E., Forge, T.A., Wu, X., 2006. Starter
phosphorus and broadcast nutrients on corn with contrasting colonization by
mycorrhizae. Agron. J. 98, 394401.
Brown, A.D., 2003. Feed of Feedback. Agriculture, Population Dynamics and the
State of the Planet. International Books. Utecht, The Netherlands, 431 pp.
Cakmak, I., 2002. Plant nutrition research: priorities to meet human needs for food
in sustainable ways. Plant Soil 247, 324.
Cordell, D., White, S., 2010. Securing a sustainable phosphorus future for Australia.
Farm Policy J. 7 (3), 117.
Cordell, D., Drangert, J.O., White, S., 2009. The story of phosphorus: global food
security and food for thought. Global Environ. Change 19, 292305.
Correll, D.L., 1998. The role of phosphorus in eutrophication of receiving waters: a
review. J. Environ. Qual. 27, 261266.
De Clercq, P., Sinabell, F., Hofman, G., Jarvis, S.C., Neeteson, J.J., Gertis, A.C., 2001.
Discussion and conclusions. In: De Clercq, P., Gertis, A.C., Hofman, G., Jarvis, S.C.,
Neeteson, J.J., Sinabell, F. (Eds.), Nutrient Management Legislation in European
Countries. Ghent University, Department of Soil Management and Soil Care,
Ghent, Belgium, pp. 307324.

830

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

De Willigen, P., Van Noordwijk, M., 1987. Roots, plant production and nutrient use
efciency. PhD Thesis Wageningen Agricultural University, Wageningen, The
Netherlands, 282 pp.
Deasy, C., Quinton, J.N., Silgram, M., Bailey, A.P., Jackson, B., Stevens, C.J., 2010.
Contributing understanding of mitigation options for phosphorus and sediment
to a review of the efcacy of contemporary agricultural stewardship measures.
Agric. Syst. 103, 105109.
Department of Commerce, 2005. National Programme for Organic Production, India
Organic, sixth ed. Ministry of Commerce and Industry, New Delhi.
Ehlert, P.A.I., Van Middelkoop, J.C., Dekker, P.H.M., 2006. Fosfaatgehalten en
fosfaatafvoer van landbouwgewassen. Rapport 1348, Alterra, Wageningen,
The Netherlands, 63 pp (in Dutch).
Erisman, J.W., 2009. Integrating nitrogen use and food production with
environmental expectations. In: Proceedings No. 664, International Fertiliser
Society, York, UK, pp. 124.
EU, 2007. Council Regulation (EC) No. 834/2007 of 28 June 2007 on organic
production and labelling of organic products and repealing Regulation (EEC) No.
2092/92. Ofcial Journal of the European Union, L 189/2.
EU, 2008. Commission Regulation 889/2008, detailed rules for the implementation
of regulation 834/2007 on organic production and labeling. Ofcial Journal of
the European Union L250, 84 pp.
Eurostat, 2010a. <http://epp.eurostat.ec.europa.eu/portal/page/portal/agriculture/
data/main_tables>.
Eurostat, 2010b. <http://epp.eurostat.ec.europa.eu/tgm/table.do?tab=table&init=
1&plugin=1&language=en&pcode=tag00091>.
Evans, T.D., 2008. Nutrient and carbon recovery from household and food
biowastes. In: Proceedings 635, International Fertiliser Society, York, UK, 124.
Fealy, R., Schrder, J.J., 2008. Assessment of manure transport distances and their
impact on economic and energy cost. In: Proceedings 642, International
Fertiliser Society, York, UK, 128.
Gerben-Leenes, P.W., Nonhebel, S., 2002. Consumption patterns and their effects on
land required for food. Ecol. Econ. 42, 185199.
Giller, K.E., Beare, M.H., Lavelle, P., Izac, A.-M.N., Swift, M.J., 1997. Agricultural
intensication, soil biodiversity and agroecosystem function. Appl. Soil Ecol. 6,
316.
Grant, C., Bittman, S., Montreal, M., Plenchette, C., Morel, C., 2005. Soil and fertilizer
phosphorus: effects on plant P supply and mycorrhizal development. Can. J.
Plant Sci. 85 (1), 313.
Heffer, P., Prudhomme, M., 2008. Medium-Term Outlook for Global Fertilizer
Demand, Supply and Trade 20082012. 76th IFA Annual Conference Vienna
(Austria), 1921 May 2008.
Hilton, J., Johnston, A.E., Dawson, C.J., 2010. The phosphate life-cycle: rethinking the
options for a nite resource. In: Proceedings 668. International Fertiliser
Society, York, UK, pp. 144.
Hooda, P.S., Rendell, A.R., Edwards, A.C., Withers, P.J.A., Aitken, M.N., Truesdale,
V.W., 2000. Relating soil phosphorus indices to potential phosphorus release to
water. J. Environ. Qual. 29, 11661171.
IFOAM, 2010. <http://www.ifoam.org>.
Johnston, A.E., Dawson, C.J., 2010. Physical, chemical and biological attributes of
agricultural soils. In: Proceedings International Fertiliser Society 675, York, UK,
pp. 140.
Jordan-Meille, J., 2009. Comparaison des methods de raisonnement de la
fertilization phosphate en Europe: quels diagnostics, pour quelles
prconisations? Actes des Rencontres de Blois des 25 et 26 novembre 2009,
Journes COMIFER-GEMAS.
Kies, A.K., Kemme, P.A., Sebek, L.B.J., Van Diepen, J.Th.M., Jongbloed, A.W., 2006.
Effect of graded doses and a high dose of microbial phytase on the digestibility
of various minerals in weaner pigs. J. Anim. Sci. 84, 11691175.
Laegreid, M., Bckman, O.C., Kaarstad, O., 1999. Agriculture, Fertilizers and the
Environment. CAB International Publishing, Wallingford, UK. 294 pp.
Letey, J., Sojka, R.E., Upchurch, D.R., Cassel, D.K., Olson, K.R., Payne, W.A., Petrie, S.E.,
Price, G.H., Reginato, R.J., Scott, H.D., Smethurst, P.J., Triplett, G.B., 2003.
Deciencies in the soil quality concept and its application. J. Soil Water Conserv.
58, 180187.
Liu, Y., Villalba, G., Ayres, R.U., Schrder, H., 2008. Global phosphorus ows and
environmental impacts from a consumption perspective. J. Ind. Ecol. 12 (2),
229247.
Lott, J.N.A., Bojarski, M., Kolasa, J., Batten, G.D., Campbell, L.C., 2009. A review of the
phosphorus content of dry cereal and legume crops of the world. Int. J. Agric.
Res., Gov. Ecol. 8 (56), 351370.
Louwagie, G., Gay, S.H., Burrell, A., 2009. Sustainable agriculture and soil
conservation (SoCo); nal report. JRC Scientic and Technical Reports EUR
23820EN, Ispra, Italy, 171 pp.
Loveland, P., Webb, J., 2003. Is there a critical level of organic matter in the
agricultural soils of temperate regions: a review. Soil Till. Res. 70, 118.
Ma, C.H., Kalb, T., 2006. Development of starter solutions technology as a balanced
fertilization practice in vegetable production. Acta Hortic. 700, 167172.
Neeteson, J.J., Schrder, J.J., Smit, A.L., Bos, J.F.F.P., Verloop, J., 2006. Need and
opportunities to reduce phosphorus inputs, soil supply and loss from
agriculture in The Netherlands. In: Proceedings 595. International Fertiliser
Society, York, UK, pp. 124.
Neyroud, J.A., Lischer, P., 2003. Do different methods to assess soil phosphorus
availability across Europe give comparable results? J. Plant Nutr. Soil Sci. 166,
422431.
OECD, 2010a. <http://www.oecd.org./tad/env/indicators>.
OECD, 2010b. <http://stats.oecd.org/Index.aspx?DataSetCode=CSP2009>.

Organic Federation of Australia, 2005. National Standard for Organic and BioDynamic Produce. 3.1 ed. As amended January 2005.
Parentoni, S.N., Lopes de Souza Junior, C., 2008. Phosphorus acquisition and internal
utilization efciency in tropical maize genotypes. Pesq. Agropec. Bras. 43 (7),
893901.
Pfeffer, E., Beede, D.K., Valk, H., 2005. Phosphorus metabolism in ruminants and
requirements of cattle. In: Pfeffer, E., Hristov, A.N. (Eds.), Nitrogen and
Phosphorus Nutrition of Cattle. CABI, Wallingford, UK, pp. 195231.
Prudhomme, M., 2010. Peak phosphorous: an issue to be addressed. Fertilizers and
Agriculture. International Fertilizer Industry Association (IFA), Paris.
Quinton, J.N., 2002. Detachment and transport of particle-bound P: processes and
prospects for modelling. In: Chardon, W.J., Schoumans, O.F. (Eds.), Phosphorus
Losses from Agricultural Soils: Processes at the Field Scale. Cost Action 832
Quantifying the Agricultural Contribution to Eutrophication. Alterra,
Wageningen, pp. 6165.
Reijneveld, J.A., Ehlert, P.A.I., Termorshuizen, A.J., Oenema, O., 2010. Changes in the
soil phosphorus status of Agricultural land in the Netherlands during the 20th
century. Soil Use Manage. 26 (4), 399411.
Richards, I.R., Dawson, D.J., 2008. Phosphorus imports, exports, uxes and sinks in
Europe. In: Proceedings 638, International Fertiliser Society, York, UK, pp. 128.
Rmer, W., 2009. Anstze fr eine efzientere nutzung des phosphors auf der basis
experimenteller befunde. Ber. Landwirtsch. 87 (1), 530.
Ruttenberg, K.C., 2003. The Global Phosphorus Cycle. Treatise on Geochemistry, vol.
9. Elsevier Ltd., pp. 585643.
Sawyer, J.E., Schmitt, M.A., Hoeft, R.G., Siemens, J.C., Vanderholm, D.H., 1991. Corn
production associated with liquid beef manure application methods. J. Prod.
Agric. 3, 335344.
Scheinost, P.L., Lammer, D.L., Cai, X., Murray, T.D., Jones, S.S., 2001. Perennial wheat:
the development of a sustainable cropping system for the US, Pacic Northwest.
Am. J. Alt. Agric. 16 (4), 147151.
Schrder, J.J., 1999. How to reduce nitrate leaching from maize land? Meststoffen
1999, Nutrient Management Institute, Wageningen, The Netherlands, pp. 67
74.
Schrder, J.J., 2005. Manure as a suitable component of precise nitrogen
nutrition. In: Proceedings No. 574, International Fertiliser Society, York, UK,
pp. 132.
Schrder, J.J., Bos, J.F.F.P., 2008. Relationships between nutrient recycling,
environmental impacts and agricultural production. In: Proceedings No. 624,
International Fertiliser Society, York, UK, pp. 128.
Schrder, J.J., Verloop, J., 2010. Slurry separation could allow a wider use of manure
within the EU Nitrates Directive. In: Cordovil, C., Ferreira, L. (Eds.), Proceedings
Ramiran 2010 Conference, Lisboa, Portugal <http://www.ramiran.net/
ramiran2010/docs/Ramiran2010_0047_nal.pdf>.
Schrder, J.J., Ten Holte, L., Brouwer, G., 1997. Response of silage maize to placement
of cattle slurry. Neth. J. Agric. Sci. 45, 249261.
Schrder, J.J., Aarts, H.F.M., Ten Berge, H.F.M., Van Keulen, H., Neeteson, J.J., 2003. An
evaluation of whole-farm nitrogen balances and related indices for efcient
nitrogen use. Eur. J. Agron. 20 (12), 3344.
Schrder, J.J., Scholeeld, D., Cabral, F., Hofmans, G., 2004. The effects of nutrient
losses from agriculture on ground and surface water quality: the position of
science in developing indicators for regulation. Environ. Sci. Policy 7 (1), 15
23.
Schrder, J.J., Cordell, D., Smit, A.L., Rosemarin, A., 2010. Sustainable use of
phosphorus. European Union Contract ENV.B.1/ETU/2009/0025. Report 357,
Plant Research International, Wageningen University and Research Centre,
Wageningen, The Netherlands, 122 pp.
Simic, D., Kovacevic, V., Simic, B., Rengel, Z., 2009. Genotypic differences among
maize inbred lines in phosphorus fertilizer responsiveness on soils differing in
acidity. Comm. Soil Sci. Plant Anal. 40, 815824.
Sinclair, A.G., Johnstone, P.D., Smith, L.C., OConnor, M.B., Nguyen, L., 1993.
Agronomy, modelling and economics of reactive phosphate rock as slowrelease phosphate fertilizers for grassland. Fert. Res. 36, 229238.
Smil, V., 2000. Phosphorus in the environment: natural ows and human
interferences. Annu. Rev. Energy Environ. 25, 5388.
Smit, A.L., Bindraban, P.S., Schrder, J.J., Conijn, J.G., Van der Meer, H.G., 2009.
Phosphorus in agriculture: global resources, trends and developments. Report
282, Plant Research International, Wageningen, The Netherlands, 36 pp.
Steen, I., 2006. Phosphorus use by livestock: requirements, efcient use and
excretion. In: Proceedings 594, International Fertiliser Society, York, UK, pp. 1
48.
Stockdale, E.A., Lampkin, N.H., Hovi, M., Keatinge, R., Lennartsson, E.K.M.,
Macdonald, D.W., Padel, S., Tattersall, F.H., Wolfe, M.S., Watson, C.A., 2001.
Agronomic and environmental implications of organic farming systems. Adv.
Agron. 70, 261327.
Stockdale, E.A., Shepherd, M.A., Fortune, S., Cuttle, S.P., 2002. Soil fertility in organic
farming systems: fundamentally different? Soil Use Manage. 18, 301308.
Stone, D.A., 2000a. The effect of starter fertilizers on the growth and nitrogen use
efciency of onion and lettuce. Soil Use Manage. 16, 4248.
Stone, D.A., 2000b. Nitrogen requirement of wide-spaced row crops in the presence
of starter fertilizer. Soil Use Manage. 16, 285292.
Syers, J.K., Johnston, A.E., Curtin, D., 2008. Efciency of soil and fertilizer phosphorus
use. FAO Fertilizer and Plant Nutrition Bulletin 18. Rome, Italy.
Tunney, H., Breeuwsma, A., Withers, P.J.A., Ehlert, P.A.I., 1997. Phosphorus fertilizer
strategies: present and future. In: Tunney, H., Carton, O.T., Brookes, P.C.,
Johnston, A.E. (Eds.), Phosphorus Loss from Soil to Water. CAB International,
Wallingford, UK, pp. 177203.

J.J. Schrder et al. / Chemosphere 84 (2011) 822831

United Nations, 2007. The 2006 Revision Population Base. <http://esa.un.org/unpp/>.
Uri, N.D., Lewis, J.A., 1998. The dynamics of soil erosion in US agriculture. Sci. Total
Environ. 218, 4558.
Van Dijk, W., 2003. Adviesbasis voor de bemesting van akkerbouw-en
vollegrondsgroentengewassen. PPO-publicatie nr. 307, Praktijkonderzoek
Plant & Omgeving, Lelystad, 66 pp (in Dutch).
Vanlauwe, B., Tittonell, P., Mukalama, J., 2007. Whitin-farm soil fertility gradients
affect response of maize to fertiliser application in western Kenya. In: Bationo,
A., Waswa, B., Kihara, J., Kimetu, J. (Eds.), Advances in Integrated Soil Fertility

831

Management in Sub-Saharan Africa: Challenges and Opportunities. Springer,

Netherlands, pp. 121132.
Verheijen, F.G.A., Jones, R.J.A., Rickson, R.J., Smith, C.J., 2009. Tolerable versus actual
soil erosion rates in Europe. Earth Sci. Rev. 94, 2338.
Watson, C.A., Bengtsson, H., Ebbesvik, M., Les, A.K., Myrbeck, A., Salomon, E.,
Schrder, J.J., Stockdale, E.A., 2002. A review of farm-scale nutrient budgets for
organic farms as a tool for management of soil fertility. Soil Use Manage. 18,
264273.