Journal of Environmental Quality SPECIAL SECTION

CELEBRATING THE 350TH ANNIVERSARY OF DISCOVERING PHOSPHORUS—FOR BETTER OR WORSE

Phosphorus Management in High-Yield Systems

Bryan G. Hopkins* and Neil C. Hansen

Abstract
The discovery and development of phosphorus (P) and P
fertilizers provide context for current management conventions.
Average crop yields were stagnant before the Green Revolution
T he discovery and development of P and P fertiliz-
ers provide context for current and future management
conventions. Understanding historical perspectives as
they flavor current thinking, despite a rapidly changing agricul-
tural world, can illuminate traditional soil P management and
but have steadily increased since. This, along with conventional
P management, has resulted in widely depleting soil P levels.
needed changes.
Improved technology and management are needed to meet
the increasing P demand. Modern hybrids and cultivars have Historical Perspectives
different P demand and uptake patterns that require changes
in conventional P fertilizer placement and timing. Phosphorus Yields and Phosphorus before the Green Revolution
fertilizer recommendations based on soil analysis remains The first agricultural revolution shifted hunter–gather soci-
valid, but evidence suggests a need for recalibrating soil test P
eties to crop cultivation. Subsequent revolutions spread species
(STP) critical levels (the STP concentration at which a response
to P fertilizer would not be expected) and P fertilizer rates to and farming techniques, resulting in widespread cultivation and
accommodate high-yield scenarios. Considering higher P fertilizer distribution of domesticated crops and increasing the land each
rates as a single solution poses environmental challenges, laborer could farm. But crop yields remained low for millennia.
highlighting the need for improved P use efficiency (PUE). Wheat (Triticum spp.) yields were ~0.5 to 1.2 Mg ha-1 in some
Phosphorus fertilization approaches that have the potential
of the earliest, rainfed agricultural communities in the Middle
to improve PUE and enable high yields include crop-specific
precision placement of P, informed timing of P fertilizers, and new East 3000 to 12,000 BP (Araus et al., 2014). Unlike more agri-
enhanced efficiency sources of P fertilizer. This paper examines culturally advanced areas, current yields in the Middle East are
these management approaches from historical, production, and roughly equivalent at 0.7 to 1.2 Mg ha-1 (Araus et al., 2014) and
environmental perspectives in modern cropping systems. were even similar to those in the United States between 1865
and 1940 at 0.7 to 1.1 Mg ha-1 (USDA-NASS, 2019).
Core Ideas Fertilization was undoubtedly initiated by ancient peoples
observing improved harvests where ash, nutrient-rich sediments,
• History of P fertilization illuminates traditional soil P manage- domestic wastes, and green and animal manures were applied.
ment and needed changes.
These observations led to rudimentary fertilization evident in
• Recalibration of STP and P fertilizer recommendations are need-
ed to match increasing yield and rates of P uptake. the archeological record (Araus et al., 2014). But the availability
• Environmental concerns and diminishing P supply necessitate of these fertilizers was minimal and management was not well
improvement in P use efficiency. understood. Other limiting factors, such as pests and weather,
• Placement and timing are improved through understanding of masked the potential benefits of fertilizer. Thus, ancient fertil-
variable rooting patterns. ization maintained the yield baseline but did not dramatically
• Enhanced efficiency P fertilizers can be effective if applied cor- increase yields.
rectly.
In fact, records at Oxford University during the 14th cen-
tury documented that yields declined below the baseline with
repeated cropping of the same soil. Continual cropping on the
same soil was routine in this region due to the limited cultiva-
tion area and large population. Scientists and farmers commonly
observed that release of nutrients through weathering of soil min-
erals and decomposition of organic matter (OM) was adequate
for native ecosystems but not enough in productive agricultural

© 2019 The Author(s). This is an open access article distributed under the CC BY-
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Brigham Young Univ., 4105 LSB, Provo, UT 84602. Assigned to Associate Editor Jim
Ippolito.
J. Environ. Qual. 48:1265–1280 (2019)
doi:10.2134/jeq2019.03.0130 Abbreviations: APP, ammonium polyphosphate; DAP, diammonium phosphate;
Received 18 Mar. 2019. EEF, enhanced efficiency fertilizer; MAP, monoammonium phosphate; NDVI,
Accepted 9 Aug. 2019. normalized difference vegetative index; OM, organic matter; PUE, phosphorus use
*Corresponding author (hopkins@byu.edu). efficiency; STP, soil test phosphorus; VRF, variable rate fertilization.

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systems as the native soil fertility was depleted ( Johnston et al., Breakthroughs in Soil Analysis and Fertilization
2014). They learned that to prevent soil degradation and asso-
The Green Revolution is indicated by the sharp and steady
ciated starvation, mineral nutrients removed through harvest
increase in yields in many nations, including the United States
needed to be replenished to sustain an agriculturally dependent
(Fig. 1). This seminal event in history was spawned by advance-
population.
ments in agricultural science and related disciplines, including
Hopkins (2015) reviewed the history of formal fertilization
pest management, irrigation, crop breeding and genetics, mecha-
science, which began in the late Renaissance with develop-
nization, communications, transportation, computerization,
ments in the core sciences, including the discovery of chemi-
and the widespread availability of inexpensive fertilizers and
cal elements. Elemental P was discovered in 1669 by Hennig
scientific knowledge related to their use, including soil analysis.
Brandt (Emsley, 2000; Sharpley et al., 2018). Emsley (2000)
Soil scientists began to successfully predict P fertilizer response
masterfully discussed the many positive and negative impacts
with soil analysis, which was an important part of this revolution
of P in society, including its role in developing agriculture and
(Anderson, 1960; Peck, 1990; Johnston et al., 2014).
as an essential nutrient for all biological life. In 1800, Erasmus
Several chemical soil extractants have been successfully
Darwin (1731–1802), grandfather of Charles Darwin, wrote
developed to measure a fraction of soil P with reasonable cor-
in The Philosophy of Agriculture and Gardening that N and P are
relation to yield and/or crop quality response to P fertiliza-
plant nutrients taken up by roots and that compost, bone ash,
tion (Mallarino, 2003; Hopkins, 2015). Correlations of soil P
and manures should be applied as fertilizers. He even suggested
extraction with crop response were reasonable and proved to be
exploration of P-bearing minerals (Darwin, 1800). Although
a valuable advance in soil fertility (Peck, 1990) and continuing
largely ignored for decades, this work eventually led to discov-
today (Mallarino, 2003; Poulton et al., 2013). These extractants
eries of P as an essential nutrient and P fertilization science.
are not perfect in their prediction of this complex relationship
Early scientists understood P was essential and commonly
and their performance varies with soil types (Heckman et al.,
deficient in soil. However, sources of P, such as manure, were
2006). For example, the Bray P1 extractant should not be used
limited. This was a large societal problem as food was some-
on calcareous soils because the carbonates neutralize the poorly
what scarce. But with the increasing scientific understanding
buffered acid extractant; rather, the Olsen bicarbonate and the
of the day, effective P fertilizers were discovered and the fertil-
Mehlich 3 extractants are much more effective for calcareous
izer industry was born, with development of widely available
soils (Mallarino, 2003; Hopkins, 2015). Appropriate soil test
effective, affordable products. As such, P fertilizer use multi-
P (STP)–based fertilizer recommendations continue to be
plied exponentially, especially during the decades immediately
important for crop production and water quality (Fulford and
before the Green Revolution in the mid–20th century.
Culman, 2018), including in high-yield environments (Boring et
However, informal observation and scientific studies revealed
al., 2018).
that fields receiving frequent P fertilizer applications in past years
The use of STP as a decision tool is widely proven and
would often no longer exhibit yield increases with continued
accepted. As with Mallarino (2003) and Sucunza et al. (2018),
P application. Hall (1909) discussed the history of P fertiliza-
the typical approach is to evaluate the P response in the year of
tion and stated that at that time, it was impossible to predict if
application. This is highly valuable information, but as society
P fertilizer application would result in a
response or not and, if it was responsive,
the proper rate to apply for each cropping
system and environment. A predictive
tool for P fertilizer recommendations was
needed, which was especially challenging
given the known complexity in soils and
cropping systems that prevented accurate
fertilizer recommendations.
Scientists worked to solve these dilem-
mas beginning in the latter half of the
19th century and into the next (Anderson,
1960; Peck, 1990). The first efforts inves-
tigated plant tissue analysis, but these were
often not adequate because P deficiency
would occur in irreversible fashion before
the test results were available and fertil-
izer could be applied (Hopkins, 2015).
Despite widespread availability of P fertil-
izer prior to the Green Revolution, grow-
ers continued to lack a reliable, predictive
tool that would inform them, before
planting, whether they should apply P
Fig. 1. Average annual yield in the United States relative to the pre–Green Revolution averages
and, if so, at what rate. (set to equal 0) of 6.4 (potato), 1.6 (maize), 1.9 (rice), 0.9 (wheat), 1.0 (soybean), and 24.8 (sugar
beet) Mg ha-1 (adapted from USDA-NASS, 2019).
1266 Journal of Environmental Quality
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moves toward higher yields there is a need to expand the view
to include the long-term approach to promote sustainable soils,
yields, and society. Most of the P taken up by a crop comes from
residual in the soil (Fixen and Bruulsema, 2014; Johnston et al.,
2014). In research trials, it is common for control plots (no P
fertilizer added) to yield reasonably well in the short term, even
with low to moderate STP (Schlegel and Havlin, 2017). For
example, Hopkins et al. (2010a, b, c) measured a significant
increase in potato (Solanum tuberosum L.) yields when P fertil-
izer was applied, but the treatments with no added P had yields
within ~90% of the fertilized ones. Note that this effect is only
with 1 yr without P (these fields received P in prior years).
Schlegel and Havlin (2017) demonstrated the important role
of residual and fertilizer P in a long-term, irrigated, continu-
ous maize (Zea mays L.) study (Fig. 2). The control treatment, Fig. 2. Annual maize grain yields for a long-term fertilizer study near
with no N and P fertilizer (0N–0P), had average yields that Tribune, KS, from 1961 to 2010. Untreated control (0N–0P; X), N
remained at background levels–despite other advances in agri- fertilizer only (179N–0P; C) at 179 kg N ha−1, and N + P (179N–20P; @)
at the same rate of N plus 20 kg P ha−1 (Schlegel and Havlin, 2017).
culture (Schlegel and Havlin, 2017). Fertilization with N and P
(179N–20P) resulted in an immediate, significant yield increase
over the control, with the average yields trending higher over High-Yield Agriculture
time. Initially, yields were similar when N was applied without Yield Trajectory Requires Phosphorus Innovations
P (179N–0P), as the maize thrived on the existing soil P. After
The upward yield trajectory for the last eight decades shows
this, P gradually depleted and yields declined significantly to the
no signs of reaching a plateau (Fig. 1). This continued pattern in
point where P became the most limiting factor in the system. The
high-yield agriculture requires understanding the highly variable
gap between adequate and absent P fertilizer widened over time
differences in total P demand and uptake efficiency across species
as residual P depleted. The STP concentration gradually reduced
and cropping systems (Hopkins, 2019).
from 17 to 6 mg P kg-1 (Bray P1) for plots receiving no P fertil-
izer over the six decades of the study. It is noteworthy that the Key Species for Examining the Yield–Phosphorus Relationship
decline in STP was not dramatic between the first year and the Given limited space herein, we selected eight representative
years when yield declines were first measured. In the absence of species for the following discussion. We based our selection on
applied P fertilizer, these plants obtained P from the natural, low- crops with global importance as well as crops that have unique
level cycling that occurs in soil. This residual P supplied enough plant–soil P relations. Grain crops are the most important glob-
to grow a base yield, but fertilizer P was necessary for elevated ally in value and acreage (USDA-NASS, 2019) and as such utilize
yields. This and similar studies demonstrate the importance of the majority of fertilizer P sold. The top four grain crops—maize,
viewing fertilization from a long-term viewpoint and gives clues rice (Oryza spp.), soybean [Glycine max (L.) Merr.], and wheat—
on how we should move forward in fertilization science. were selected for discussion (Table 1). In addition, potato and
Understanding the role of soil and fertilizer P was vital in apple (Malus pumila Mill.) are the most globally important veg-
obtaining the steadily increasing yields through the Green etable and fruit crops, respectively. Finally, onion (Allium cepa
Revolution. One important concept going forward is under- L.) and sugar beet (Beta vulgaris L.) are globally significant and
standing the relationship between P soil supply and plant are included as key species as they represent unique root systems
demand. The transformation of solid phase soil P to plant-avail- and P relations. Each of these that have reliable long-term yield
able forms can be described in one of two processes: decompo- histories show an increase in relative yield (average for the last
sition of organic materials and solubilization of P containing decade compared with the baseline in Fig. 1 at 638, 522, 327,
minerals. The rate of microbial decomposition of crop residues 241, 215, 172% for potato, maize, rice, wheat, soybean, and
or soil OM is largely independent of the rate of P uptake by sugar beet, respectively). Historical yield records for onion and
plants—with both similarly dependent on soil temperature apple are not as reliable (and therefore not shown in Fig. 1), but
and other factors. This is similar for the rate of dissolution of evidence shows upward yield trajectories (Lazicki et al., 2016;
P-containing minerals, although equilibrium chemistry will USDA-NASS, 2019). The upward yield trajectories and unique
result in a slightly elevated dissolution rate as soil solution P soil–plant P relations in these eight species, which are largely rep-
concentration drops. However, the bottom line is that the rate resentative of the diversity of crops found in the world, warrant
at which P is converted to plant-available forms in the soil is further examination of the role of P in high-yield agriculture.
not proportionally linked to uptake rate. In other words, supply Cropping Systems Outpace Fertilizer Recommendations
will not completely keep pace with demand, and therefore, new
and innovative ways to enhance supply need to be established as Initially, crops were fertilized very similarly regardless of spe-
demand for P increases due to increasing yields. Although adding cies. With time, individual nuances with species, and even within
high rates and building the labile and nonlabile P fractions will species, were realized and custom fertilization resulted in ben-
improve supply, it is often not enough to meet the high demands efits. The past several decades have seen significant advances in
of high yield agriculture (Hopkins, 2015). soil, nutrient, and fertilizer sciences. However, the approach to
manage P fertilizers has also remained largely similar. The primary

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Table 1. Categories of row crops (underlined), along with select species, with annual global acreage and value (Food and Agriculture Organization,
2019). The species shown represent those selected for further evaluation in this paper based on their global importance, as well as an effort to iden-
tify contrasting P needs.
Species Scientific name Crop category Acreage Value
10 ha
6
109 US$
Grain 1086 1258
Rice Oryza spp. Grain 192 367
Maize Zea mays L. Grain 211 274
Wheat Triticum spp. Grain 244 211
Soybean Glycine max (L.) Merr. Grain 115 112
Other Grain 325 293
Annual fruit/vegetable 182 1070
Potato Solanum tuberosum L. Annual vegetable 24 123
Onion Allium cepa L. Annual vegetable 6 52
Perennial fruit/vegetable 93 498
Apple Malus pumila Mill. Perennial fruit 7 81
Sugar 32 128
Sugar beet Beta vulgaris L. Sugar 5 13
Nuts 44 92
Fiber 40 69
Other 35 92
Total of categories 1512 3207

method of fertilization for most growers involves soil analysis to other aspects of modern cropping systems changed dramatically.
determine the P rate with application based on one of the follow- Changes (such as new crop cultivars and hybrids, new fertilizer
ing approaches: (i) applying a sufficient amount of P to maximize materials and application methods, and even changes in soil and
the economic return of the fertilizer in the year of application, climate conditions) may require adaptation of fertilizer strategies.
(ii) maintaining P by applying the amount of P removed by the Fulford and Culman (2018) called into question the suitability
crop, or (iii) applying an excess of P to build up the STP and then of current fertilizer P recommendations aimed at maintaining
applying a maintenance amount once STP reaches a high level STP due to higher yielding systems. They stated that the recom-
(Olson et al., 1982). Dry fertilizer (most commonly diammo- mendations require updating to better reflect fertilizer needs
nium phosphate [DAP] or monoammonium phosphate [MAP] with modern maize and soybean productions systems. Heckman
is broadcast applied and incorporated into the soil with tillage. et al. (2006) took a similar view, pointing out a need to at least
Growers in high-yield environments will often apply a liquid fer- apply a removal rate of P to soils that are not excessively high
tilizer in a concentrated band near and/or on the seed or seed in STP. Hopkins et al. (2018) conducted a meta-analysis with a
piece (Borges and Mallarino, 2001; Rosen et al., 2014; Preston et variety of crops, with results suggesting P responses at STP con-
al., 2019). In reduced tillage systems, ammonium polyphosphate centrations higher than typical critical levels.
[APP] is commonly dribbled in a concentrated band on the soil Yields Are Largely Proportional with Phosphorus Demand
surface or, more effectively, injected into the soil near the seed
(Preston et al., 2019). These practices remain the standard means Increases in overall biomass clearly result in increases in the
of P management despite dramatic changes in yields. amount of P in that biomass. Although concentrations are vari-
These traditional P management approaches are insufficient able by species, plant part, and development stage (Table 2), every
as standalone techniques in high-yield systems (Hopkins, 2019). plant cell contains P. Despite these differences in plant tissue P
While the principles and practices are still relevant, many gen- concentration, that variation is less important than variation in
erally accepted soil critical levels and corresponding fertilizer crop yield when determining total P requirements (Wortmann
recommendations remained unchanged over decades while et al., 2018). Table 2 shows that a majority, although not all, of

Table 2. Phosphorus uptake (International Plant Nutrition Institute, 2014), average crop yields (Lazicki et al., 2016; USDA-NASS, 2019, averaged
across 2007–2016), P removal at average yields (USDA-NASS, 2019), leaf P concentrations (Bryson et al., 2014), and P concentrations in the harvested
portion (Lardy and Schafer, 2014; USDA-ARS, 2019; USDA-NRCS, 2019) for eight key species.
Uptake Yield Removal Leaves Harvested portion
kg P Mg -1
Mg ha -1
kg P Mg -1
kg P ha
-1 % %
Potato 0.92 46.9 0.56 26 0.20–0.50 0.04
Maize 4.19 10.1 2.70 27 0.25–0.50 0.21
Rice 3.67 8.2 2.54 21 0.10–0.18 0.10
Wheat 5.24 3.1 3.83 12 0.20–0.50 0.42
Soybean 7.86 3.1 6.48 20 0.25–0.50 0.70
Sugar beet 0.61 64.6 0.45 29 0.45–1.10 0.24
Onion 0.21 56.6 0.14 8 0.35–0.50 0.03
Apple 0.25 34.8 0.04 2 0.10–0.40 0.01

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the P taken up by plants is removed at harvest for most annual
species. The P is mobile within the plant, and much of it is trans-
ported to the harvested portion as plants approach maturity.
As such, the amount of P taken up and removed from a field
is strongly coupled with yield. As average yields for a variety
increase, P demand also increases. For example, potato P uptake
rates and total uptake were strongly related to yield (Horneck,
2004; Stark et al., 2004). Stark et al. (2004) reported that ‘Russet
Burbank’ potato with yields of ~50 Mg ha-1 has a maximum
daily P uptake rate of ~0.42 kg ha-1 d-1 with a total seasonal P
uptake of ~33 kg ha-1. In an area with a longer growing season
and, thus, higher yield potential, Horneck (2004) reported a
56% higher yield (~78 Mg ha-1) for the same cultivar, with a
total P uptake 121% higher (73 kg ha-1). The difference in P
uptake was not only a factor of a longer growing season; the daily
P uptake rate was also proportionally much higher, at a 138% Fig. 3. Estimated cumulative P uptake for maize as a function of grow-
increase (0.90 kg ha-1 d-1). Bender et al. (2013a) reported on the ing degree days (GDDc) for maize growth with vegetative (V) and
work of earlier researchers showing P uptake in maize of 24, 34, reproductive (R) stages shown for “modern hybrids” (adapted from
Bender et al., 2013a) and “older hybrids” (adapted from Ritchie et al.,
and 70 kg P ha-1 for yields of 4.6, 6.3, and 16.3 Mg ha-1, which 1997).
were nearly proportional increases in P uptake per megagram of
grain increase. Karlen et al. (1987a, 1987b, 1988) discussed P soybean took up 23 to 32% of its total P uptake during the repro-
uptake and partitioning in maize being related to yield. ductive stages of growth (R1–R5.5), with a very strong relation-
Although P uptake and removal will increase somewhat ship between P uptake and yield across several varieties and site
proportional to yield, there are differences within species for P years. Advanced P management in high-yield systems demands
removal. Gill et al. (2004) reported that while most of the 30 an understanding of the P uptake patterns by the cultivars and
wheat varieties they evaluated had similar grain P concentra- hybrids being grown.
tions, some were dissimilar. Bender et al. (2013a) estimated 40% The top end of yield potential is unknown (Bender et al.,
of the increase in P uptake for modern maize hybrids is due to 2013a). The highest documented yields achieved are approxi-
advances in cultural techniques, such as increased plant popula- mately double the average yields at present for most crops, which
tions, but that the rest is due to genetic improvements. suggests that technology and genetic improvements can lead
In addition to genetic advances in crop yield, modern hybrids to continued yield increases and the corresponding need for
and cultivars often exhibit different P uptake patterns than former improved P management and supply. The average maize yields
hybrids and cultivars. The rate of P uptake over the growing reported over the last decade are ~10.1 Mg ha-1 (Fig. 1), but
season for maize hybrids of the past generally follows an S-shaped growers and researchers have reported yields in the range of at
curve, with minimal P uptake during emergence and early growth least 20 to 25 Mg ha-1. Similarly, average potato yield is 46.9
(V5–V8 stages), followed by a rapid rate of uptake through the Mg ha-1 (Fig. 1), but maximum yields of over twice that have
remaining vegetative growth stages, and then a period of slow been achieved. Average wheat yields are 3.1 Mg ha-1 (Fig. 1), but
P uptake from the R1 to R6 stages while the grain is filling and irrigated high-yield wheat commonly reaches three times these
maturing (Fig. 3). Modern hybrids have a modified uptake pat- values. A similar situation exists for most other crops, with a
tern as they continue to take up P at high rates through the R1 documented large potential for increased yields.
to R6 growth stages, with minimal reduction in P accumulation As innovations create ever-increasing yields, it is essential
rate at the end of the season (Fig. 3). Bender et al. (2013a) noted to understand the relationship between increasing yield and P
that modern maize hybrids have increased the accumulation of demand and removal with a modernized approach to crop-specific
P, with the maximum accumulation rate occurring at the V10 to management of soil P and P fertilizers. The yield trajectory in Fig.
V14 growth stages at 1 kg P ha-1 d-1, but with uptake rates nearly 1 is expected to continue for many years to come. These contin-
as high over a relatively longer time postflowering when most of ued increases require greater demand for P. But adding higher and
the P is taken up. Therefore, the total demand for P for the season higher rates of P to meet crop demand is problematic. Higher rates
is much higher at 47 to 58 kg P ha-1 reported for modern hybrids hasten the depletion of P-containing ores, natural gas, and other
with relatively high yields compared with older hybrids at 24 to resources used in their manufacture and transportation (Hopkins,
34 kg P ha-1 (Bender et al., 2013a). In a similar study, Bender et 2015). In addition, there are potentially negative environmental
al. (2013b) found that new hybrids have 10% higher yields and impacts with high P rates (Hopkins, 2015). It is critical to under-
12% greater P uptake. Woli et al. (2017) also showed that modern stand advanced techniques in P soil–plant relations to meet P
maize hybrids have relative greater P uptake, with a strong propor- demand with sophisticated sources, timing, and placement.
tional relationship between biomass and grain yield.
Similarly, Julia et al. (2016) showed that a large percentage Modernizing Proven Practices
(40–70%) of P uptake occurred late in the season (after flower- Soil Test Phosphorus Critical Levels
ing) for modern rice cultivars. Gill et al. (2004) found similar Critical levels for STP are determined experimentally, with a
differences across wheat cultivars, although there was variability significant body of information available with good correlations
in the ratio of yield to P uptake. Gaspar et al. (2017) showed that to yield response for reliable extractants, such as in the work of
Journal of Environmental Quality 1269
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Mallarino (2003) and Sucunza et al. (2018). Fixen and Bruulsema for P fertilizer for crops in that region needed a substantial
(2014) stated that responses to P fertilizer are seldom observed upward adjustment. This was likely due to higher yields with asso-
above 45, 30, and 23 mg P kg-1 for the most commonly used ciated higher demand for P and changing cropping patterns (e.g.,
extractants (Mehlich 3, Bray P1, and Olsen bicarbonate, respec- potato, a high P-demand crop, was being grown more frequently
tively). Fertilizer P is recommended at STP concentrations below in the rotations). In many fields, P application was not keeping
these critical levels and none when above them. Applying P to pace with removal, leading to depleted soil conditions. They also
plants in excess of need has led to decreases in growth (Thornton found that P rates needed to be based on yield potential and, in an
et al., 2008, 2014; Barben et al., 2011; Nichols et al., 2012; unprecedented advancement in the science of fertilization, that
Hopkins, 2015). Additionally, soils in great excess of the STP the rates needed to be adjusted on the basis of concentration of
represent an increased environmental risk for transport of P to free carbonates in the soil. As a result, the new recommendations
surface water bodies (Hansen et al., 2002; Sharpley et al., 2018). for P fertilizer rate applied to potato (Russet Burbank) for a stan-
Although these principles are accepted, there is a question dard yield of 45 Mg ha-1 grown on soil with 10 mg kg-1 Olsen
regarding the reliability of STP critical levels that are based on bicarbonate extractable P with 0% free carbonates is 180 kg P2O5
lower yields of the past. Syers et al. (2008) noted the importance ha-1, which is significantly higher than the previous recommen-
of accurate critical levels for modern production. Many fertilizer dations (Stark et al., 2004). Further refinements showed that if
P recommendations based on STP do not consider the expected the yield potential were significantly higher at 80 Mg ha-1, the
yield in the recommendation. The greater P uptake and removal rate would increase to 265 kg P2O5 ha-1. If the soil is calcareous,
due to increasing yields has the twofold effect of raising the total with 12% limestone, the rate would increase to 400 kg P2O5 ha-1
P demand and, if soil is under fertilized, depleting residual soil P. at the higher yield. This is an excellent, albeit rare, example of the
For these reasons, yield-based adjustments in STP critical levels type of adjustments needed in all cropping systems as yield levels
and P fertilizer recommendations are needed. continue to climb.
Although adding large amounts of fertilizer P in a single Additional evidence of the need to adjust STP critical levels is
application to correct a low STP is common practice in some demonstrated in a meta-analysis of a wide variety of crop species
cropping systems, especially with alfalfa (Medicago sativa L.) and and soils with responses to traditional and enhanced P sources
other perennials, adding extremely high rates of P in any one measured at STP levels higher than traditional critical levels
year does not completely overcome the effects of a depleted soil. (Hopkins et al., 2018). Yields increased with P fertilization an
Rather, maintaining an adequate STP is recommended as a strat- average of 7% for the lower STP categories. Although lesser in
egy to sustain high yields (Mallarino, 2003; Poulton et al., 2013). magnitude, yield also increased 5% for the higher STP categories
However, current trends in agriculture are in the opposite above the critical levels. Most of the positive responses at high
direction ( Johnston et al., 2014). Nutrient removal rates exceed STP were in the high, but not excessively high, levels, especially
replacement applications in most areas, as evidenced by steadily with crop species with unusually high P demand (e.g., potato).
declining soil test values (International Plant Nutrition Institute, Grain and most other crops did not give a P response at the very
2015). A broad analysis of millions of commercial agricultural high STP values, and many had negative yields as a function
soil test results in North America between 2001 and 2015 shows of P fertilization in very high STP soils (likely due to induced
that STP concentrations have decreased (Fig. 4). Most areas have deficiencies of micronutrients). Notably, the upper range for
diminishing STP, although the opposite often occurs in areas responsiveness to P fertilization for the four most common
with a relatively high ratio of manure to land available for appli- STP extractants was 55, 40, 40, and 30 mg kg-1 for the Mehlich
cation (Pizzeghello et al., 2016). The combination of increasing 3-ICP, Bray P1, Mehlich 3-colorimetric, and Olsen bicarbon-
yields (Fig. 1) and nutrient-depleted soils (Fig. 4), with a con- ate extractants, respectively. These values are ~22 to 33% higher
stant eye on the cost–benefit relationship, results in a need to than the typical published STP critical values reported by Fixen
adjust fertilizer recommendations associ-
ated with critical levels of STP as the crop-
ping systems change and develop.
There is a need to increase P supply in
high-yield environments, although it must
be done efficiently ( Johnston et al., 2014;
Reid et al., 2018). Critical levels for STP
and P fertilizer rates and/or efficiency
need to increase as a function of yield
and the associated increase in P demand
(Wortmann et al., 2018). It is not benefi-
cial to build STP to excessively high levels;
rather, P potentially should be applied at
concentrations higher than in the past.
Tindall and Stark (1997) reported on Fig. 4. Change in the distribution of soil test P (STP) categories using data between 2001 and 2015
an example of these adjustments with a based on millions of North American soil analyses (International Plant Nutrition Institute, 2015).
university–industry cooperative effort. Upward bars indicate that over the time period, there are higher percentages of soil samples
The key finding was that the STP critical within that STP range. Downward bars indicate a smaller percentage of samples within that range.
Overall, the figure shows a P depletion trend because soils with STP of less than 20 mg kg−1 Bray P1
levels and the associated recommendations are increasing in frequency and soils with STP values greater than 20 mg kg−1 are decreasing.
1270 Journal of Environmental Quality
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and Bruulsema (2014). The high STP concentration at which environmentally friendly (Hopkins, 2015) or economically
responses were routinely observed strongly suggests a need to sustainable (Hopkins et al., 2007). Increasing P fertilizer rates
increase STP critical levels in response to increasing yields and as the only adjustment will not likely be sufficient to keep pace
STP depletion. The adjustments need to be tailored to specific with extremely high uptake rates and modern cropping systems
soil, crop, and environmental conditions. This is especially true criteria.
in cropping systems where the P removal rate is higher due to A preferred solution is to focus on improving fertilizer P
removal of straw, stalks, and other aboveground biomass for use efficiency (PUE). To accomplish this goal, it is necessary to
animal feed, fuel production, and so on. understand P uptake and removal rates (demand; Table 2) and
Foundational Management Principles for High Yields the interaction of plants with soil physical, chemical, and biolog-
ical properties (supply), along with understanding the interface
Growers and society need to synergistically balance environ- between plant and soil—the root system. Using this informa-
mental and economic issues to achieve sustainability of farms tion, P fertilizer management can be fine-tuned—including
and the planet. The 4R approach to nutrient management has species–specific precision placement and enhanced efficiency
been advocated in recent years. This refers to applying the (i) fertilizer (EEF) sources.
right fertilizer source at the (ii) right rate at the (iii) right timing
in the (iv) right placement (Bruulsema et al., 2012; Bruulsema, Spatially Precise Technologies
2017; Flis, 2018). The 4R framework is intended to be compat- Variable rate fertilization (VRF) is a best management prac-
ible with social, economic, and environmental outcomes, with tice for P fertilizers in most agricultural fields (Lal and Stewart,
each considered in nutrient decisions. Scientifically based best 2015; Shannon et al., 2018). Although it may seem like a basic
management practices for financial, pest, water, soil, and nutri- practice, VRF application in P management is often not per-
ent management need to be viewed and studied as interacting formed correctly. High-yield systems often benefit from proper
factors rather than as stand-alone practices. Bruulsema (2017) VRF management of P, determined separately from N and K.
briefly listed management practices for many of major commod- Identifying P management zones is often done best with bare soil
ity crops, while Flis (2018) discussed those specifically related imagery, where differences in topsoil and carbonate concentra-
to P. Hopkins (2019) built on these in systems with high yield tions are often readily visible, along with topography, soil depth,
potential to include, although not limited to the following: historical field information (especially manure), soil-borne pest
• Select appropriate solid and/or liquid sources with high history, yield map and canopy health (measured via normalized
availability of P to plants. vegetative difference index [NDVI]) history, and intensive sam-
• Account for degradation rates of crop residues and animal pling with chemical, physical, and microbial analysis (especially
wastes, especially in cool soils. lime content, pH, OM).
• Account for the possible value, synergy, and/or toxicity of Another advanced technique used in high-yield systems is the
accompanying nutrients and other chemicals in the fertilizer accurate placement of fertilizer bands (Lal and Stewart, 2015;
blend. Shannon et al., 2018). Accurate placement is especially beneficial
• Avoid unwanted precipitation or caking or clumping during when these bands are applied at a different time than planting.
handling. Modern technology with tractors that are driven precisely with
GPS can very accurately place the fertilizer in relation to seed/seed
• Correct and/or account for soil pH and other chemical
piece location, so that the band is not too close to or too far from
properties of soil and their interaction with fertilizers.
the planted rows, which is discussed in more detail below. Such
• Use appropriate P fertilizer rates based on scientific and/or
accuracy can be a vital component of achieving superior yields.
on-farm studies (P response and/or omission plots) specific
to the P source, soil, and cropping system. Variable Root Access to Phosphorus
• Use tissue analysis to evaluate fertilizer effectiveness with, Although Weaver (1926) and Weaver and Bruner (1927)
if needed, rescue applications of P appropriate for the emphasized the importance of root systems nearly a century ago,
cropping system, followed by adjustments in preplant experience and a search of the literature shows that little effort
fertilization in future years. has been spent in understanding the detailed architecture and
• Evaluate root growth and vascular system health to morphology of the root systems of modern hybrids and cultivars
determine the effectiveness of this aspect of the P supply because root excavation and mapping is painstakingly slow and
system for the plant. difficult (Ordóñez et al., 2018). Nevertheless, having at least a
Although these practices are traditional, it is important to build a rudimentary understanding of root development patterns for
high-yield system on the proven foundation of these long-stand- each species (preferably each cultivar and hybrid) in unique
ing tenets of soil fertility (Hopkins, 2019). In addition, we must cropping systems is one of the most important keys for P man-
evaluate the interactions between them, as well as incorporate agement in efficient, high-yield systems.
sophisticated sources and technologies discussed below. Because P is a poorly soluble nutrient, P uptake is primarily
through root interception and short-distance diffusion (Fixen
Meeting Increased Phosphorus Demand and Bruulsema, 2014; Johnston et al., 2014). This limits the per-
Exceptional Yields Require Exceptional Management centage of soil supplying P to roots. Thus, the interface between
the soil and root system is complex, but it is critical to under-
Moderately increasing STP levels and P fertilizer rates may
stand for superior P management as our knowledge of rooting
be necessary to prevent depleting soils of P, but rate increase
patterns is improved.
alone and building STP to extremely high levels may not be

Journal of Environmental Quality 1271

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Root systems are affected by a variety of factors, including, Thornton et al., 2008, 2014). Each plant species listed in Table 1
but not limited to, row widths, within-row plant spacing, pre- has unique root systems and P physiology, as well as the soil types
vious crops, tillage system, soil bulk density, and crop species they are typically grown in and the soil–root interface.
and hybrid/cultivar. Competition with neighboring plants can Root Morphology and Architecture of Key Species
reduce rooting efficiency. Root exploration can be hampered sig-
nificantly if the cropping system results in excessively high soil Maize has a larger biomass accumulation than most other
bulk densities and poor oxygen content. However, the dominant annual crops, which equates to high total P uptake (Table 2).
factor affecting root development is genetics (Iwama, 2008; Despite the high demand, it is efficient at P uptake because the
root system is wide (~2.5 m) and deep (~2.3 m) (Fig. 5a). The

Fig. 5. Relative shoot and root sizes at early stages of growth (~60 d) and near maturity for (a) onion, sugar beet, potato, soybean, spring wheat,
rice, and maize and (b) apple. Adapted from Weaver (1926), Weaver and Bruner (1927), Atkinson and Wilson (1980), Atkinson (1983), Yamaguchi
and Tanaka (1990), Thorup-Kristensen (2006), Iwama (2008), Andresen et al. (2016), Fan et al. (2016), and Ordóñez et al. (2018).

1272 Journal of Environmental Quality

 15372537, 2019, 5, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.2134/jeq2019.03.0130 by INASP/HINARI - AFGHANISTAN, Wiley Online Library on [01/09/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
massive soil exploration by roots with many root hairs enables Yamaguchi and Tanaka (1990) and Iwama (2008) reviewed
maize to have a high PUE. insights into root systems and show similar findings as Weaver
Wheat is a relatively smaller plant with a narrow but deep (1926) and Weaver and Bruner (1927), but with greater quantifi-
root system (Fig. 5a), with ample root hairs and uptake effi- cation. Among the six crop species compared in side-by-side trials,
ciency. Despite its overall lower demand for P per plant relative potato had the lowest root density by a substantial margin. The
to maize, its limited root system grown in relatively cooler soils average density for the potato root system was one-fourth of that
make wheat somewhat more responsive to P fertilizer (Yaseen et measured for wheat. Low root density certainly appears to be a
al., 2017; Sucunza et al., 2018). factor in the high soil solution P requirements of potato. Sirisena
Soybean is similar to wheat in biomass (Fig. 5a). Like wheat, and Suriyagoda (2018) noted that potato was much more respon-
soybean has a much smaller aboveground biomass than maize, sive to P fertilizer than maize, soybean, and onion, which were
but Ordóñez et al. (2018) found that the maximum depth of much more responsive than rice grown in flooded soils.
roots was greatest for soybean (1.7 m, with 95% within 1.4 m), Onion has a smaller root system than even potato (Fig. 5a).
followed by wheat (1.5 and 1.0 m), and maize (1.2 and 0.9 m). Its root cylinder has a very small diameter and, thus, does not
Soybean was also greatest in terms of root density in the P-rich explore much soil. But, opposite of potato, it is a small plant
topsoil, with 50% of roots in the top 0.11 m, compared with and as such has a very low P demand (Table 2). As Boyhan et
maize and wheat at 0.14 and 0.17 m, respectively. This, along al. (2007) noted in their review, P relations in onion are not
with lower biomass, helps explain why soybean is relatively less well studied, and the few published studies they found included
responsive to P fertilization (Boring et al., 2018). Many growers only a few documented responses. The study by Jha et al. (2000)
do not apply P fertilizer directly to soybean. Rather, they apply showed limited response with uptake of P in onion, while the
a slight excess of P to its rotational partner(s), commonly maize study by El-hamady (2017) showed significant response to P
(Boring et al., 2018). This is reported to be effective in some cases fertilizer with onion. Andresen et al. (2016) noted that onion
but not so in others (such as with high-yield soybeans and when roots grow slower and have less lateral root development than do
STP is low (Boring et al., 2018). They found that maize was rela- wheat and lettuce (Lactuca sativa L.), with less rooting equaling
tively more responsive than soybean and stressed the importance less nutrient uptake. They also found differences among cultivars.
of accurate STP interpretive levels. Thorup-Kristensen (2006) found that the rate of root growth
Rice is also similar to wheat and soybean, with relatively low was four to six times lower for onion than other vegetables and,
aboveground biomass. As with soybean, it has an extensive and at harvest, onion was found to be shallow‐rooted, with a final
effective root system (Fig. 5a). However, rice is often grown in rooting depth of only 0.3 m, whereas lettuce was 0.6 and carrot
saturated soils. Flooded soils result in changes in the redox chem- (Daucus carota spp.) and cabbage (Brassica oleracea L.) reached
istry, which has the net effect of increasing the solubility and rooting depths of at least 1.1 m. Another important factor with
plant availability of P (Patrick et al., 1985). As such, rice tends onion is its mutualistic relationship with mycorrhizae fungi
to be less responsive to P than most other crop species when (Brown, 2001). Most crop species can benefit from this symbi-
grown in saturated conditions (Sirisena and Suriyagoda, 2018). otic relationship. Mycorrhizae effectively extend the root system,
Yadvinder-Singh et al. (2000) compared P fertilizer and STP for increasing water and nutrient uptake and other reported ben-
a wheat–rice cropping system and found the wheat response to efits. This relationship can be important for most of the species
be typical but showed that the availability and STP were much discussed herein, especially with onion, but with sugar beet as
higher when the soil was in a saturated condition growing rice. an exception. However, ample water and nutrition, tillage, and
They and Baskar et al. (2000) reviewed studies showing similar fumigation all reduce the reliance on this relationship. Brown
relations. Rice grown in nonsaturated conditions behaves simi- (2001) found that fumigation resulted in P deficiency—presum-
larly to other grain crops, although there are differences in root ably from a negative impact on the mycorrhizal relationship—
systems that affect P relations. but that it was overcome through broadcast and/or incorporated
Potato exhibits a vastly different soil–root P relationship than P fertilization when nonfumigated onions were not responsive
the grain crops (Fig. 5a). Rosen et al. (2014) noted that potato (presumably due to mycorrhizae).
has a relatively high fertilizer P requirement and exhibits yield Sugar beet is an example of a species with even more distinc-
increases at greater STP than other species. Potato tends to have tive soil–root P relations. It has a very limited root system early in
a shallow root system, which is relatively less efficient due to low the season but eventually develops to thoroughly explore the soil
density and few root hairs (Iwama, 2008; Fixen and Bruulsema, (Fig. 5a). Sugar beet has a strongly dominant taproot that focuses
2014; Mikkelsen, 2015). As Thornton et al. (2014) noted, potato on downward growth for the first 8 to 12 wk. As such, it primar-
has shallow roots with relatively less root length and hairs than ily explores the subsoil early in the season, which typically has
sugar beet and, especially, wheat. Additionally, potato has a large very low STP. Sugar beet sets its yield potential during this time
demand for P (Fixen and Bruulsema, 2014; Rosen et al., 2014). by determining the number and thickness of the cambial rings
Because of these factors, potato has a much higher P requirement that store sugar in the taproot (Stevens et al., 2007). If there is any
and a lower PUE than most other crops (Fixen and Bruulsema, type of stress, the yield potential can be irrevocably lowered even
2014). As such, it tends to respond to P at much higher STP if growing conditions are ideal later in the season. Eventually, in
than other crops and requires rates two to three times greater the mid to late season, sugar beet roots begin to grow horizon-
than most other crops (Fixen and Bruulsema, 2014; Rosen et tally and explore the nutrient-rich topsoil (Fig. 5a). But that may
al., 2014). The most commonly grown potato cultivar, Russet be too late if the plant underwent P-deficiency stress during the
Burbank, requires much more P than some newer developed cul- early season. As such, early-season P management is relatively
tivars (Thornton et al., 2008, 2014). critical—with placement based on root architecture being vital.
Journal of Environmental Quality 1273
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Apple is yet another species with unique soil–root P rela- increasingly high in PUE. Additionally, there is also a need for
tions (Fig. 5b). As a tree crop, it has an extensively wide and deep efficiency of the P in the plant material being fed to livestock for
root system. Apple and many other perennial woody species are environmental factors (Raboy, 2002). Although there have and
grafted onto various roots stalks, including those of other species, will continue to be changes, the relative differences between spe-
which makes understanding its rooting system somewhat com- cies first demonstrated by Weaver (1926) and Weaver and Bruner
plex. As Atkinson and Wilson (1980) noted, results of P fertil- (1927) are similar today, as shown by Iwama (2008). These
ization vary depending on cultivars and root stocks. Many of the researchers show root length density by depth. This density in
roots are found in P-depleted subsoil. The distribution and activ- the topsoil (0–10 cm) was in order of rice > wheat > sugar beet
ity of apple tree roots are 1 to 2 m deep, with some reports show- > maize = soybean > potato. Relative density distributions for
ing depth equal to height and a lateral spread two to four times these species were similar in the soil just below this layer (10–20
canopy diameter (Atkinson, 1983). As with all perennial crops, cm), although maize and soybean root densities were relatively
it is especially important to incorporate nutrients with limited higher than in the top 10 cm. Below this, densities declined,
mobility in the soil, such as P, into the soil at planting. After this, with potato having very low densities relative to the other crops.
tillage is not recommended, which makes moving P into the deep Rooting depths were wheat > maize > sugar beet > soybean >
soil difficult. However, once a tree is mature and fruit bearing, it potato = rice. One notable change is that high-yield systems
already has much of its biomass with associated P established. often include increased plant populations with associated reduc-
Much of the P in leaves is mobilized and stored in the wood and tions in overall root biomass. For example, Li et al. (2019) found
then remobilized to leaves the next growing season. Therefore, its that an increase in maize population by one-third decreased root
uptake rates are low. The studies by Nava et al. (2017) and Stiles biomass 26 to 32%.
(1994) showed no response to P for apple. Neilsen et al. (2008) Table 3 further demonstrates these important differences.
noted that apple has very low demand for P and that historically Yamaguchi and Tanaka (1990) found that the root system was
studies showed no response to added P. However, they showed shallower in rice and deeper in maize than in the other crops.
increased P uptake and 20% yield increase with P fertigation Soil depth where 90% of the roots was distributed was 0.23 m
across several cultivars in their own work. They stated that P is in rice, 0.35 to 0.38 m in potato and soybean, 0.48 to 0.51 m
especially needed when its root system is unusually limited, such in sugar beet and wheat, and 0.59 m in maize. The root density
as with newly planted or replant disorders and with low STP. (value of various root traits per unit soil volume) in the upper
Undoubtedly, the rooting patterns discussed here have soil layers and the largest density observed among various soil
changed somewhat since Weaver (1926) and Weaver and Bruner positions were larger in rice and wheat and smaller in potato and
(1927) did their classic work. For example, the new ‘Alturas’ soybean. Fan et al. (2016) reviewed a wide variety of crops and
potato cultivar has a much more efficient root system than Russet found similar results for wheat, maize, and soybean (they did not
Burbank, one of the oldest cultivars and the one most widely report on the other key species discussed herein).
grown in the United States. This improved efficiency allows for Efficient P use depends on understanding the unique rooting
improved water and nutrient uptake. In this case, Alturas goes patterns for each species, as well as hybrid and cultivar differences
against the trend of needing more P as a function of relatively and impacts as a function of cropping and tillage systems which
greater yields because the improvement in PUE is so enormous. affect compaction and other soil properties. Understanding root-
Thornton et al. (2008, 2014) pointed out the need for continued ing patterns and the associated physiology related to P is instruc-
genetic improvement, suggesting improvement strategies with tive with regard to P placement in relation to the rooting system.
genetic developments, especially root health (mass, depth, and Phosphorus fertilizer strategies for modern crop production
susceptibility to pests and pathogens) as a solution to improve should consider the crop-specific P uptake patterns. Both potato
PUE in potato, with newer cultivars having much higher PUE (Hopkins, 2015) and onion ( Jha et al., 2000) need season-long,
than Russet Burbank (up to twice as much), but higher inter- steady supply of P to maximize yields and, more important,
nal P requirement. In addition, White et al. (2018) found that ensure crop quality. Grain crops, especially modern hybrids and
increased juvenile root vigor accelerated P acquisition and initial cultivars (Bender et al., 2013a) are similar, although less sensi-
canopy cover and, thereby, increased tuber yields and that juve- tive. In contrast, sugar beet takes up a large percentage of its P by
nile root vigor is a heritable trait and can be selected to improve the time it closes the canopy and is very sensitive to deficiencies
the P-fertilizer use efficiency of potato. early and not nearly as much late in the season (Hopkins, 2015).
These principles are similar for other species. Crop breeders Apple, as a perennial tree crop, has a very low P demand—taking
and geneticists need to develop cultivars and hybrids that are up and storing P over many years.

Table 3. Comparison of root characteristics throughout the soil profile at the stage of maximum shoot growth for six species (adapted from
Yamaguchi and Tanaka, 1990).
Dry weight Length Surface area Volume Average diameter
gm -2
km m -2
m m
2 -2
×10 cm m
3 3 -2 mm
Maize 316 50 88 12.9 0.56
Wheat 247 89 98 9.1 0.36
Rice (flooded) 203 78 86 7.6 0.35
Soybean 152 39 48 4.8 0.39
Sugar beet (excluding tap root) 114 52 64 6.5 0.39
Potato 61 21 22 1.8 0.33

1274 Journal of Environmental Quality

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Placement and Timing Considerations of P, the P is more soluble. The concentrated band is much more
The placement and timing of P fertilizer applications are man- effective when injected into the root zone than as a surface band
agement variables that significantly influence PUE. Common P (Borges and Mallarino, 2001; Preston et al., 2019). Typically, a
fertilizer application placements, listed in decreasing order of broadcast application incorporated into the soil has an average
PUE, include (i) concentrated bands in root zone, (ii) broadcast PUE across a variety of crops of only ~5 to 10% in the first year
and incorporated, (iii) surface concentrated bands (including after application, but it increases to ~30 to 35% with a concen-
drip fertigation), (iv) injection into overhead irrigation (ferti- trated band in the root zone. Syers et al. (2008) and Johnston et
gation), (v) foliar sprays, and (vi) surface broadcast, not incor- al. (2014) thoroughly reviewed crop PUE, citing single-year P
porated. The PUE varies for each, with effectiveness generally recovery from fertilizer often lower than 10%, but they suggested
greatest with injected concentrated bands and decreasing in the it could be as high as 90% over the long-term. Wortmann et al.
order listed. Selection of P fertilizer placement has generally (2018) stated that maize yields could be greater with higher-
been driven by compatibility with tillage practices, but seeking than-recommended STP when springs are relatively wet and
high PUE in modern, high-yield systems requires better match- cool with minimal root growth and slow soil chemical and bio-
ing of P fertilizer placement with specific crop and variety root- logical activity. Band applications near the seed greatly help in
ing patterns and with soil P physical chemistry. overcoming these early-season challenges.
The importance of application placement and timing of P Although concentrated bands are most efficient for single-year
fertilizer is unique among macronutrients due to its distinctive uptake of P, the likelihood of salt, ammonia, and other damage to
physical chemistry reactions in soil. Growers and their advisors newly emerged plants greatly limits the rate that can be applied
often mistakenly assume that P should be managed similar to N. in direct seed contact (noting that no liquid should be applied
Nitrogen is vulnerable to leaching and gaseous losses and, thus, directly to some species, such as potato). However, this danger
often benefits from in-season applications over earlier ones. In diminishes with distance to the concentrated band. For most
contrast, P does not have loss mechanisms to the atmosphere species, a higher rate of fertilizer can be applied if the distance
and is much less vulnerable to leaching. At very high STP (typi- is 5 cm to the side and 5 cm below the seed for crops with typi-
cally due to very high rates of manure and similar materials), P cal diagonal root patterns (Fig. 5). Achieving high yields requires
will leach downward (Pizzeghello et al., 2016; Neidhardt et al., understanding of root morphology and architecture to influence
2018). High STP also results in P losses in runoff (Hansen et al., the ideal position of banded P fertilizer. For example, a band of
2002; Sharpley et al., 2018). However, in most soils, P is gen- fertilizer directly below the seed is often a key to obtaining high
erally not very mobile in soil ( Johnston et al., 2014). As noted yields for sugar beet, even in soils with high STP (Hopkins and
in Pierzynski and Hettiarachchi (2018), P from liquid fertilizer Ellsworth, 2005; Ellsworth and Hopkins, 2006; Stevens et al.,
sources is more mobile than P from dry fertilizer sources, which 2007; Moore et al., 2009). For sugar beet, the widely promoted
is helpful for moving P into the soil after surface applications. diagonal placement of N, and especially P, to the side of the seed
Hill et al. (2015a, b) showed that APP liquid was more mobile is ineffective (Anderson and Peterson, 1978; Stevens et al., 2007;
than MAP—moving it several centimeters away from point of Hopkins and Stephens, 2008; Sims, 2010). As the taproot grows
application when applied in a concentrated band, especially rapidly and the seedling is salt sensitive, using a low to moderate
when blended with an organic acid. They found that this resulted P rate placed 0.05 to 0.15 m directly below the seed is important.
in increased P uptake and yield. Montalvo et al. (2015) found Unlike potato and most other crops, small deviations in the side-
differences between fluid and dry P mobility but suggested that to-side placement for sugar beet can negate the benefit (Stevens
there was no agronomic benefit in soils in which P availability is et al., 2007; Hopkins and Stephens, 2008). Correct placement
controlled by strong adsorption. Although P may be relatively enables the plant to set a high yield potential and supplies the
more mobile in certain liquid forms than in dry fertilizer, it is plant with needed P (and other nutrients) for the first ~60 to
still relatively less mobile than most nutrients, including N and 70 d when its root system is focused on exploration of the nutri-
K. The placement and timing of P fertilizer needs to account for ent depleted subsoil. While less research is available, it is likely
the principles of poor P mobility in soil. that a similar outcome would be observed for other species with
prominent taproots, such as alfalfa and carrot. This is in contrast
Concentrated Bands Near the Seed to other species, such as wheat and canola, where placement
In general, concentrated bands provide the most efficient of P is best to the side and down from the seed (Grant et al.,
applications of P (Grant et al., 2001; Hopkins et al., 2010b, 2001). Maize, rice, soybean, and onion also have diagonal roots
2014; Rosen et al., 2014; Withers et al., 2014). This is especially that benefit with side band placement. Precise band placement
true with low STP and with cool soil conditions. Randall and depth for potato is not as critical as for other species due its lack
Vetsch (2008) found that placement of concentrated bands was of sensitivity to P deficiency during emergence and to the long,
needed, especially with low STP, in strip-till with maize–soy- belowground stem from which roots grow, as long as the place-
bean systems, and they cited similar findings for other cropping ment is to the side of the seed piece and not on it or below it (Fig.
systems. Grant et al. (2001) found similar with high-yield wheat 5a; Hopkins and Stephens, 2008).
and canola (Brassica napus L.) in soils that were low in STP and Banded P placement is similarly effective with most other spe-
cool due to early planting. cies (Borges and Mallarino, 2001; Grant et al., 2001; Preston et
It is imperative that the band stays intact during planting al., 2019). These are especially important with high-yield no- or
and other possible soil disturbances, which is especially a con- minimum-tillage cropping systems and especially after multiple
cern with potato and other deeply planted species (Hopkins and years (Hansen et al., 2002; Preston et al., 2019). Tillage warms
Stephens, 2008). By maintaining a high, localized concentration soils and, as such, aids in P uptake. Tillage also enables placement
Journal of Environmental Quality 1275
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of P in the root zone. These advantages are lost in pure no-till sys- at times there is benefit to building soil fertility with broadcast
tems, which often results in P stratification with P concentrated applications when STP is low.
at the soil surface (Smith et al., 2017). Using sophisticated appli- To achieve high yields, the crop needs to begin the season
cation equipment that minimally disturbs crop residues and soils with a high probability of having ample P throughout. But
with P injection into the root zone using GPS guidance at the despite best efforts, P supply is sometimes not sufficient and
correct distance and direction of the seed is an essential practice in-season “rescue” applications, although not ideal, are needed.
for high-yield systems where P is deficient (Preston et al., 2019). Deficiencies of P are most evident in the cool, early spring.
Seed-propagated species with diagonal growing roots, such as the Although some species (such as sugar beet, onion, rice, and
grain crops, perform best when the concentrated band is near, apple) are not very susceptible to mid- to late-season deficien-
but away from, the seed at 0.05 m to the side and down from the cies, others (especially potato and maize) are extremely sensitive
seed for optimal root access soon after emergence. to P deficiency in high-yield situations (Bender et al. (2013a,
Concentrated Bands on the Seed b); Hopkins, 2015). It is a best management practice to moni-
tor plant tissues for all crops in-season (Bryson et al., 2014). The
In addition to understanding rooting patterns, one must also recommended tissue to be sampled varies by species and growth
address P physiology when making P timing and placement deci- stage (Bryson et al., 2014). For example, maize ear leaf samples
sions (Grant et al., 2001). Planting dates are often early in the are taken, whereas petioles are taken with sugar beet. Samples are
season in an attempt to lengthen the growing season to obtain taken as frequently as needed, often weekly. This is especially the
high yields. As a result, soils are relatively cool, with associated case for sensitive species, with the trend in rate of concentration
slow root growth and soil biological and chemical processes that decline often more important than a value at a single point in
affect P availability. Given low P concentrations in the seed and time (Stark et al., 2004).
minimal P uptake, a low-rate, low-salt “starter” fertilizer in direct Precision management of the zones with varying properties
seed contact often helps with early-season P needs. The smaller is needed for in-season management (Lal and Stewart, 2015;
the seed, the greater the need. Relative seed/seed piece sizes are Shannon et al., 2018). Zonal in-season soil and/or plant samples
potato >> maize > soybean > wheat = rice > onion = sugar beet along with remote sensing (via satellite, aircraft, drone, or hand-
(apple is propagated by asexual grafting). However, the smaller held devices) can potentially identify problems in real time.
the seed, the greater the salt sensitivity. Thus, maize will tolerate However, it should be noted that P deficiencies are not always
a higher rate of starter fertilizer than sugar beet. Sugar beet seed- identifiable through the canopy (Hopkins, 2015). Crop stress
lings are highly salt sensitive. They will tolerate and often benefit can also be detected by NDVI (Lal and Stewart, 2015; Shannon
from a low rate of fertilizer applied in direct seed contact if the et al., 2018). However, NDVI does not currently distinguish
soil and/or irrigation water are not too saline. between water, N, and other stresses, although there is progress
Fertilizer placement on the seed is not always helpful, how- in this area of research. Another method that is especially effec-
ever. For example, the timing and placement of P fertilizers is tive to identify P deficiency is the use of visual aerial images at
different for potato due to relatively large seed pieces. Given a the time of first canopy closure. Areas of fields where plants are
typical planting rate of 2.2 Mg ha-1 and P concentration (Table stunted and, therefore, not closing the canopy quickly are pos-
2), the seed pieces contain ~1.3 kg P ha-1, which is ample P for sibly P deficient. This can often be verified through plant tissue
early-season needs. As such, no starter fertilizer placed on the analysis.
seed piece is needed, whereas species planted with a relatively The critical value for P deficiency in plant tissues is not known
small seed often benefit from this practice. Although potato for all species but has been determined for others. For example,
is responsive to concentrated P fertilizer placed 0.08 m to the potato is responsive to in-season application of P when tissue
side of the seed piece where it accesses the P long after initial analysis shows that the petiole P concentration is forecast to drop
growth, there is no benefit to placement on the seed (Hopkins below 1700 mg kg-1 (Stark et al., 2004). In the absence of critical
and Stephens, 2008). Onion, which has a very low seedling P value data, Bryson et al. (2014) listed commonly measured values
demand, is another example of a crop for which direct seed con- for a vast array of crops and other species. Otherwise, locally col-
tact is often not beneficial. Early-season nutrition can be aided lected data for the specific soils and varieties grown are needed to
with a starter and/or a diagonally placed P band, but responses determine if a response to in-season P fertilization is likely.
are relatively less common than with most other crops (Boyhan Hopkins et al. (2010b, c) showed that potato responded to
et al., 2007). Therefore, while application of P on the seed is rela- both fertigation and preplant incorporation of P but that the
tively greater with high-yield, early-planted systems, an under- latter was more efficient for P uptake and yield response because
standing of P supply and demand during the seedling phase is the poor solubility of P causes fertigation applied P to remain
critical in making this decision. close to the surface and away from a majority of roots (Fixen and
Broadcast Incorporated, Fertigated, and Foliar Applications Bruulsema, 2014; Rosen et al., 2014). Although not as efficient
The scientific literature and grower experience are replete as soil incorporation, fertigation did result in a yield response for
with evidence of responses to broadcast P application, although potato because it has a critical mass of surface-feeding roots and
these are far more effective when incorporated into the soil a moderately wide surface footprint of just over 1 m (Fig. 5). The
( Johnston et al., 2014). If incorporation is not possible, liquid surface roots are relatively more effective once canopy closure is
fertilizers (APP) are more mobile in soil than dry (MAP, DAP), achieved (Hopkins, 2015) and if the soil has adequate moisture
especially when blended with an organic acid (Hill et al., 2015a, (Weaver, 1926)—promoting increased root growth and
b). Although concentrated P bands have relatively high PUE, interception and faster diffusion rates. Fertigation applications

1276 Journal of Environmental Quality

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can work with other species as well if there are active surface time of risk for precipitation reactions (Sharma, 1979). The most
roots. These are often absent if the surface soil is very dry. commonly used slow release forms of P are manure and other
Foliar applications designed to deposit P on the leaves have organic materials. Any structurally bound P found in these mate-
been shown to help in rescue situations, but compared with appli- rials is released during decomposition. These can be used effec-
cations directly into the root zone, they are relatively ineffective. tively when locally available and affordable or when crops to be
Foliar applications are especially needed when conditions arise grown are organically certified (Hopkins and Hirnyck, 2007).
due to unusually high growth rates and/or problems with root– Struvite, a recycled biosolid, is one example of a slow
vascular system health that may warrant application of foliar or (delayed)-release EEF P (Rech et al., 2019). Theoretically, stru-
fertigation P in rescue scenarios when tissue analysis shows P vite’s low water solubility preserves it until root acid exudates
deficiency. For example, Atkinson and Wilson (1980) showed dissolve it. The freshly dissolved P is less likely to precipitate and
increased P uptake and yields with foliar P application to fruit more likely to be taken up by roots in close proximity—result-
trees, although they stated that the path through soil is the main ing in improved P uptake efficiency. Struvite has been shown to
source of P uptake. Girma et al. (2007) showed foliar response be effective in increasing uptake and yield (Withers et al., 2014;
in maize. Fageria et al. (2009) reviewed foliar fertilization in Fisher et al., 2019; Woolley et al., 2019).
crop plants and stated that P is not applied foliarly as frequently Other examples of EEFs include organic acids blended or
as N, suggesting that this is so because of low leaf area early in bonded with P fertilizer. Although a wide array of these sub-
the season when P deficiencies are more common and because stances are abundant in the OM fraction of soil (>22,000 kg ha-1
many P fertilizers have poor water solubility. Nevertheless, they per 1% OM), evidence suggests that directly blending or bond-
reported limited responses to foliar P fertilization. Garcia and ing these with P fertilizer can increase solubility and uptake, with
Hanway (1976) conducted a variety of studies with maize and resulting increases in crop yield (Tan, 2003; Hill et al., 2015a, b);
soybean with foliar P. Results were mixed and often unpredict- Summerhays et al., 2015). The probability of response increases
able but nevertheless showed potential. Presently, there is not a in soils having poor P solubility and with reduced rates of P fer-
strong set of data supporting foliar P as a prominent component tilizer (Hopkins, 2015) and at low soil OM (Summerhays et al.,
for P management; rather, it should be relegated to a rescue role 2015). Hopkins (2015) reported an average yield increase of 7%
if needed. This may change in the future as P demands continue over a wide variety of crops. This effect was only achieved on
to increase with increasing yields and as sources and application low-OM, calcareous soils with low to moderate STP and when
methodology become increasingly sophisticated. using a reduced rate of fertilizer (when compared to a full rate of
Enhanced Efficiency Fertilizer Sources and Rates traditional P fertilizers; Fig. 6). Summerhays et al. (2017) found
that the effect was due to P uptake and not some other bios-
As previously mentioned, increasing P demand results in a timulation impact from the organic acids. However, Olk et al.
need for increasing rates of traditional P fertilizers. However, (2018) reported that these acids often resulted in biostimulation
this alone is not the best approach to advanced P management of growth, frequently with increased root growth and less com-
in high-yield systems. Increasing efficiency of applied P fertiliz- monly with a yield increase, but suggested that the effect was not
ers is a means of limiting the need for higher application rates related to P nutrition in relatively higher OM, lower pH soils.
and can reduce the environmental risks associated with high P
application rates. There are a variety of P sources
with proven enhanced efficiency (Hopkins et al.,
2008; Hopkins, 2015). While a thorough review
of these is not possible in this space, the follow-
ing are offered as examples.
It is important to understand the reasons why
a nutrient source is not efficiently taken up by
plants. The primary reasons for poor efficiency in
N are atmospheric losses and leaching, while for
K, it is primarily fixation into certain soil miner-
als. Phosphorus is unique from the other macro-
nutrients in that its inefficiency is primarily due
to fertilizer P precipitating as low-solubility min-
erals (Hopkins, 2015). Fertilizers with enhanced
efficiency seek to increase P solubility for ade-
quate movement through soil and into roots.
One simple mechanism of EEF is slow- or
control-release materials (Nyborg et al., 1995;
Yaseen et al., 2017). These materials typically
have a coating of some type, such as a polymer,
which provides slow or controlled release of the
Fig. 6. Relative yield increases (averaged over 38 studies with potato, maize, sugar beet,
fertilizer. The delayed release results in metering and wheat) with an enhanced efficiency P fertilizer additive (Carbond P) to traditional
out the nutrients to the plant over time. In the (nonorganic acid) fertilizers with identical nutrient concentrations. The Carbond P resulted
case of P, this slow or control release reduces the in a significant increase (signified by *) over the traditional fertilizer when applied at the
full rate, but the response was relatively larger when evaluated at a half rate.
Journal of Environmental Quality 1277
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Another P EEF is a maleic polymer that is blended with tradi-
tional fertilizers (Hopkins, 2013). Hopkins et al. (2018) reviewed
and conducted a meta-analysis of 503 field sites across a wide
variety of crops and soils with this polymer. It is shown to affect
soil chemistry, although the effects are variable and somewhat
uncertain (Hopkins et al., 2018; Pierzynski and Hettiarachchi,
2018). Hopkins et al. (2018) showed that many of these sites
were nonresponsive, while others had a significant response. The
overall response to this additive when blended with traditional P
fertilizer was a 2.1% increase in yield. When eliminating sites not
likely to give a P response (i.e., excessively high STP, neutral soil
pH, and high P fertilizer rates), the average response increased to
over 5%. As the STP methods used were variable in these studies, Fig. 7. Relative yield response over a wide range of crops for an
each STP value was converted to a common scale with 14 catego- enhanced efficiency P fertilizer additive (AVAIL) and the same source
of fertilizer applied at the same rate without AVAIL. The responses of
ries (1 = very low; 14 = extremely high). 503 field sites are shown as a function of 14 categories of soil test P
It is important with all of these EEFs to not apply P in cir- (STP) ranked from very low (1) to extremely high (14) (based on the
cumstances when there would not be an expected response to P International Plant Nutrition Institute [IPNI] rankings—adapted from
Hopkins et al., 2018).
fertilizer. Deciding what this critical level should be is compli-
cated by the evidence presented herein that these levels should Conflict of Interest
be adjusted upward. However, there is clearly an upper limit at The authors declare no conflict of interest.
which an EEF is no longer beneficial and possibly even detrimen-
tal (Fig. 7; Hopkins et al., 2018). Acknowledgments
We would like to acknowledge McKayla Sundberg for her artist work
Conclusions in helping to create Fig. 5. We would also like to acknowledge Tyler
Hopkins for his assistance in literature review and editing.
While crop yields remained largely unchanged through agri-
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