Phosphorus

Authored by: Bryan G. Hopkins

Handbook of Plant Nutrition

Print publication date:  May  2015
Online publication date:  May  2015

Print ISBN: 9781439881972
eBook ISBN: 9781439881989
Adobe ISBN:

10.1201/b18458-6

 

Abstract

John Emsley (2000) states “… phosphorus was greeted with great acclaim, and yet it was damned from the moment it was born.” Emsley artfully and accurately tells the history of the 13th element to be discovered—ranging from its toxicities and dangers in weaponry and industry to its nutritional role.

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Phosphorus

3.1  Historical Background

John Emsley (2000) states “… phosphorus was greeted with great acclaim, and yet it was damned from the moment it was born.” Emsley artfully and accurately tells the history of the 13th element to be discovered—ranging from its toxicities and dangers in weaponry and industry to its nutritional role.

Elemental phosphorus (P), discovered about 1669, exists in white or red mineral forms and is a multivalent, pnictogen (nitrogen family), nonmetallic element with the atomic number 15. Due to its high reactivity, it never is found naturally as a free element on Earth, but only in its maximally oxidized and hydrated state as inorganic orthophosphate (PO4 3−), or more typically associated with one or two protons as HPO4 2− or H2PO4 . The degree of protonation is a function of pH. Phosphate is a trivalent resonating tetraoxyanion that acts as a linkage or binding site and is typically resistant to polarization and nucleophilic reaction, except in metal–enzyme complexes (Clarkson and Hanson, 1980).

Presently, the vast majority of commercially produced P compounds are consumed as plant fertilizers.

Rocks and soil minerals, which contain plant nutrients in their makeup, break down very slowly, but this process is generally not sufficient to raise crops continuously. The art of fertilizing with ash, manure, salts, plant residues, etc., began shortly after the first hunter-gatherers converted their lifestyles to cultivate crops. The science of fertilization began with the discovery of various chemical elements and observations that maintaining or improving crop yields required various chemical inputs.

Emsley (2000) discusses record keeping at Oxford University during the fourteenth century, documenting the decline in yields with the constant cropping necessitated by the small land mass and the large population of England. This loss in yield is attributed to declining soil fertility. Although soils tend to be able to sustain slow to modest plant growth in native ecosystems, lost mineral nutrients must be replenished under the more intensive systems required for sustaining a population consuming agricultural commodities. Phosphorus is one of the minerals most commonly depleted to a point of significantly impacting plant growth.

Although farmers commonly observed plant response to manures and other fertilizer materials and soil amendments, the formal science of soil fertility and plant nutrition was meager prior to the late Renaissance, after which developments in biology, chemistry, and physics resulted in a series of important discoveries that eventually led to the Green Revolution of the Twentieth Century. In the early nineteenth century, Arthur Young described possibly the first formal fertilization experiments with poultry manure, gunpowder, charcoal, ashes, and salts in the Annals of Agriculture. In 1799, Erasmus Darwin, grandfather of Charles Darwin, wrote in The Philosophy of Agriculture and Gardening that nitrogen (N) and P are plant nutrients taken up by roots and that compost, bone ash, and manures should be applied as fertilizers. He even suggested exploration of P-bearing minerals. According to Emsley (2000), he was largely ignored until decades later.

About the same time, Theodore de Saussure (1767–1845) built upon discoveries by Antoine Lavoisier (1767–1845) in chemistry—confirming that plants absorb specific mineral elements from the soil. Georges Ville (1824–1897) was possibly the first to state that plants take up P in the oxidized form as an essential nutrient. Justus von Liebig (1803–1873) maintained that the “other” mineral nutrients, especially P, were as important as N, carbon (C), hydrogen (H), and oxygen (O). He popularized the Liebig’s Law of the Minimum, which actually originated with Carl Sprengel’s (1786–1859) “theory of minimum”—stating that any nutrient in deficient supply becomes the limiting factor for growth, even if the others are supplied in abundance. Liebig also built upon the work of the French chemist Jean-Baptiste Boussingault (1802–1887), who established the first agricultural experiment station in 1836—making significant advances including promotion of simultaneous application of both N and P. Hall (1909) provides an excellent review of the discoveries of these and other early scientists regarding the essentiality of plant nutrients and the developments in the fertilizer production industry.

Although the essentiality of P as a nutrient was known, the plant availability of P from limited sources other than organic wastes, such as manure, was problematic. It was learned that every living thing contained relatively high amounts of P and that the concentration in bones was especially high. However, application of pulverized bones to soil was not efficient due to the poor solubility of the calcium phosphate compound found therein. In 1840 in Germany, Liebig applied sulfuric acid (H2SO4) to powdered bones, showing that the resulting product was more successfully taken up by growing plants than untreated bone powder. This fertilizer material was termed single superphosphate (SSP; 16% to 20% P2O5), also known as normal or ordinary superphosphate.

Shortly afterward, John Bennet Lawes (1814–1900) began the testing and commercial production of mineral P in England. Although not as well documented or known, James Murray of Ireland purportedly had developed his own version of an effective P fertilizer prior to Liebig or Lawes. He and Lawes filed for patents about the same time, but Lawes eventually purchased Murray’s patent. In collaboration with others, Lawes conducted extensive research efforts at his estate, the now renowned Rothamsted Research Experiment Station, established in 1843 and the longest continuously run station. Several phosphate-containing materials (including animal manures and acidified bones and minerals) were evaluated as fertilizers at Rothamsted. These efforts launched the widespread production and use of effective phosphate fertilizers. These early P fertilizer materials frequently were mixed with N-rich bat guano and/or potassium (K) sources. Manufacturers of fertilizer sprouted up around the world in the latter half of the nineteenth century and the early twentieth century.

Interestingly, although credited with the formal discovery of acidifying bones to create a P fertilizer, Liebig lambasted England for robbing European battlefields, such as Waterloo, and catacombs in various countries of skeletons to feed the ever-increasing demand for increased agricultural productivity (Hall, 1909)—actions that provide some context for the great increase in the demand for P fertilizer during that time. Because of eventual scarcity and the associated costs of bone recovery, and with advances in the processing of apatite or rock phosphate, the practice of applying acidified bone powder largely was abandoned.

Rock phosphate was first used about 1850 to make P fertilizer, and following the introduction of the electric submerged-arc furnace in 1890, elemental P production switched from bone-ash heating to production from mineral P sources. After the depletion of world guano sources about the same time, mineral P became the major source of phosphate fertilizer production. Eventually, H2SO4 was replaced with phosphoric acid (H3PO4) to create fertilizer with a higher concentration of P, known as triple superphosphate (TSP; 0-45-0, N-P2O5-K2O) or treble, double, or concentrated superphosphate. In the 1960s, ammonia (NH3) was reacted with H3PO4 to form monoammonium phosphate (MAP; 11-52-0), diammonium phosphate (DAP; 18-46-0), and ammonium polyphosphate (APP; 10-34-0 or 11-37-0) used commonly today (Mortvedt et al., 1999; Wagganman, 1969). Phosphate rock production greatly increased in the mid-twentieth century, and it remains the primary global source of P (Figure 3.1). Phosphate mines are on every continent, with the United States, China, Morocco, and Russia recognized as the top producers.

Crop responses to P fertilization were widespread at experiment stations around the world as well as readily observed by farmers. Lawes and others at Rothamsted began what was to become a global use of the scientific method to address the need for increased crop production. Lawes and scientists at other locations conducted P fertilizer rate studies with the goal to determine the correct amount to apply. In general, these resulted in curvilinear yield responses with increasing P fertilizer rate up until yield plateaued or even declined at excessively high rates. Although rate studies were vital in guiding farmers to apply sufficient, but not extreme amounts of fertilizer, Hall (1909) discusses that it was not possible at that time to find the correct rate for all soils and circumstances. Early scientists collectively found a limit to fertilizer response by plants. The massive responses to P fertilizer reached a plateau as a result of continued P fertilization and buildup in the soil. Efforts were then concentrated upon methods of determining which plants in which soils would be responsive to fertilizers as well as the economics of fertilization.

The phosphate-rich minerals of the park formation at the Simplot Vernal Mine near Vernal, Utah, United States.

Figure 3.1   The phosphate-rich minerals of the park formation at the Simplot Vernal Mine near Vernal, Utah, United States.

Farmers and scientists understood that customized P fertilizer recommendations were needed. Initial efforts were focused on attempts to correlate plant response to P fertilizer with the total elemental concentration in soils, but it was soon discovered that the relationship was not predictive. Hall (1905) proposed plant analysis as a tool to predict fertilizer need. Macy (1936) established the notion of a critical concentration range for each species. Good correlations between plant tissue and yield were achieved for many elements and species. This tool continues to be developed and used. However, P deficiencies, especially for annual plants, often occur very early in the season before tissue can be used to predict P response. And there is convenience of being able to apply fertilizer prior to planting, thus creating a need for a predictive soil test. Therefore, initial failures in soil testing were reexamined.

Scientists studying soil physical chemistry discovered the various mineral and organic P compounds in the soil and their variability in solubility and plant availability. Several soil tests were developed with the intent to provide a reasonable correlation between yield parameters and a diagnostic determination of a P concentration related to plant P availability (Bray and Kurtz, 1945; Dyer, 1894; Hanlon and Johnson, 1984; Morgan, 1941; Olsen et al., 1954; Truog, 1930). Early reviews of plant nutrition and soil–plant relationships are made by Kitchen (1948) and Russell (1961).

The Green Revolution was a function of a wide variety of societal advancements, including advances in pest management, irrigation, crop breeding, mechanization, communications, transportation, and, especially, the advent of soil testing and the widespread availability of inexpensive fertilizers and scientific knowledge related to their use. Unfortunately, the widespread use of fertilizer did not come without its problems. In recent years, the effect of nutrient enrichment of surface water bodies has been attributed mostly to use of manures and fertilizers. There are concerns as well about the depletion of P mineral reserves. These issues have resulted in farmers, industry professionals, and scientists working toward the more efficient use of P in order to provide the food, fuel, and fiber for seven billion plus people on Earth while minimizing the impact to the environment and loss of natural resources. The remainder of this chapter is focused upon an understanding of P as an essential nutrient and its efficient use as a fertilizer.

3.2  Uptake of Phosphorus By Plants

3.2.1  Soil–Plant Interactions Impacting Uptake

Plant P uptake is relatively less efficient compared with most other nutrients due to its poor solubility in soil. Soil chemistry, discussed in more detail in a later section, has a large impact on P uptake. Plants have to “drink their nutrients” and, as such, these elements must be dissolved into the soil solution for uptake to occur. Once in solution, nutrients are taken up by plants as a function of a combination of root interception, diffusion, and mass flow.

Mass flow is the simple process of dissolved nutrients being carried in the stream of water moving through the soil and to plant roots. For nutrients that are poorly soluble in soil, such as P, mass flow is not a major contributor to uptake because of the very low concentration in the soil solution. The concentration of P in solution, even in fertile soils, rarely exceeds 1 mg kg−1 and commonly is less than 0.05 mg kg−1. This small amount of dissolved P does move via mass flow into the root apoplast. However, it is well documented that this minuscule amount of P is not adequate for intensive crop production, as plants need large quantities of this primary macronutrient.

Mass flow is a passive process, with nutrients being carried into the plant as a function of water relations. Plants, however, need a higher amount of nutrients than is supplied via this mechanism. Therefore, plants actively select and take up many of the nutrients they need—including P. This process creates a zone of nutrient salt depletion in the 0.2–1 mm rhizosphere zone near plant roots. The gradient of high salt concentration in the bulk soil compared to the lower levels in the rhizo-sphere is not chemically stable, and as a result, dissolved ions will move from the area of high salt concentration toward the area of low concentration in order to achieve equilibrium, thus hastening the movement of nutrients toward plant roots. This process of diffusion is relatively more important for P because mass flow contributions are minimal. Barber (1980, 1995) calculates that diffusion provides ~92.5% of P compared with only about 2.5% for mass flow. However, this percentage is impacted by crop species and by many soil factors, including temperature, water, P buffering capacity, and pathway tortuosity (Barber, 1977).

The remaining 5% of P uptake is attributed to root interception. However, although diffusion of P is important, continual root expansion is vital for nutrient uptake (Kissel et al., 1985; Lindsay, 2001; Marschner, 2012; Sposito, 2008). Phosphorus can diffuse only about 0.5 mm and the efficiency of diffusion in any one locale decreases as the supply of easily solubilized P is exhausted quickly. Although Barber (1980, 1995) claims that root interception is a very small contributor to P uptake, the reality is that root interception is a vital partner with diffusion and separating these two mechanisms gives a flawed view of nutrient uptake.

As roots encounter new areas of soil, they exert a considerable impact on the rhizosphere, which then affects the availability of P and other nutrients. One of the main impacts is on soil pH, with roots exuding protons and organic acids that lower pH in the rhizosphere. This action can be especially important for releasing P bound by calcium (Ca) and magnesium (Mg), especially in alkaline and calcareous soils. Acidifying fertilizers and soil amendments can have a similar impact in the soil immediately surrounding these compounds. These impacts on soil pH are localized, with the bulk soil pH not generally changing significantly in any one growing season. Organic acids, such as citrate and oxalate, exuded from roots (and microorganisms) also can displace P from soil minerals via ligand exchange, making it available for plant uptake. Again, all of these mechanisms are partners with mass flow, diffusion, and root interception in aiding in P absorption.

Hopkins et al. (2014) review the impacts on plant P availability as a function of modifications for the rhizosphere by plants and by management impacts, including pH. In the case of strongly acidic soils, it is helpful to raise soil pH to near neutral (pH 7) to maximize plant P availability and uptake. Growing at an optimum pH has other health benefits for plants, except for species that require acidic soil conditions, such as blueberry (Vaccinium spp. L.) and azalea (Rhododendron spp. L.). Similarly, most strongly alkaline pH soils are known to have limited P solubility compared with neutral to slightly acidic soils, with the exception of Chernozems, which are high in humus.

Adjusting acidic soil pH is well studied and commonly performed. Adjusting the pH of alkaline soil is also possible with the addition of elemental S, H2SO4, and other strong acids and acid- forming materials (Horneck et al., 2007). However, it is not practical to attempt to modify the pH of alkaline soils in most circumstances, especially when there is a superabundance of carbonate (CO3 2−) as in calcareous soils and in most irrigation water. In these cases, the rates of acidifying materials required are exorbitantly high and the CO3 2− buffers the pH against change. The exudation of protons by plants and microbes, fertilization (especially with ammonium (NH4 +)-based materials), and the replacement of bases (Ca, Mg, Na, and K) with H from natural precipitation and pure sources of irrigation (snow melt and other low EC waters) all work constantly to acidify soil, but the reality is that in most cases in alkaline soils, the balance lies in favor of CO3 2− accumulating in soil and preventing pH change from occurring. Therefore, the management strategy for alkaline soils is to add relatively higher rates of P fertilizer [along with other nutrients that are similarly impacted by high pH, such as zinc (Zn)] and to select species adapted to these soils rather than attempting to lower the bulk soil pH.

Although lowering the pH of alkaline soil is not practical in most circumstances, another approach to enhance P solubility is pH modification of soil microsites in the rhizosphere. Fertilization in a concentrated band with strongly acid P fertilizers, such as H3PO4, temporarily lowers the microsite soil pH in the band and can result in short-term increased P-use efficiency (PUE). However, the soil pH rebounds after a few wetting–drying cycles (Thien, 1976), and the long-term precipitates that eventually form may be even less soluble than those formed after traditional sources of fertilizer are applied (Lindsay, 2001). Furthermore, the lowering of the pH of alkaline soil using strong acids can have a negative impact on P solubility if the pH is swung too far in the other direction and an acidic soil condition occurs.

The rate of many of these chemical, and all biological, reactions is impacted by temperature. As such, the occurrence of P deficiencies is often a function of time of season. Deficiency is relatively more common early in the growing season when soils are cool and root growth is minimal. As the soil warms, the rates of most reactions in soil, roots, and microbes increase and quicken the release of P from soil minerals and organic matter and, simultaneously, roots explore new areas of soil (Gardner, 1984; Lingle and Davis, 1959; Locascio et al., 1960; Lorenz et al., 1964). This temperature effect can relieve early-season P deficiency due to these multifaceted impacts, but often the damage is done and not recoverable. Phosphorus deficiencies can also become relatively common in the late season as pathogen infection of root and vascular tissues occurs and/or root growth slows due to a shift in plant resources being applied to reproductive tissue growth.

3.2.2  Absorption of Phosphorus by Roots

In general, nutrient uptake is greatest in the region just behind the calyptra (hardened root cap) of actively growing roots where root hairs exist (White, 2012a). Root hairs serve as extensions of the epidermal cells and effectively increase the absorptive surface area of the roots. Ernst et al. (1989) found that P uptake in soil-grown corn (Zea mays L.) was reduced as distance from the tip increased. However, Clarkson et al. (1987) found that this trend could be reversed in barley (Hordeum vulgare L.) when grown under extreme P deficiency. In addition, the surface area can be further increased in many plant species through symbiotic association with mycorrhizal fungi (Hopkins et al., 2014; Robinson, 1986). These fungi penetrate root cells and their long-stranded bodies extend into the soil several centimeters past the root rhizosphere. Mycorrhizae facilitate water and nutrient uptake and are especially beneficial in the uptake of P. The presence of root hairs and mycorrhizae extends the diameter of the nutrient uptake cylinder around each root; however, it is noteworthy that the vast majority (~99%) of soil volume remains unexplored, even by species with high root length density (Fixen and Bruulsema, 2014).

Once P encounters the exterior root surface, it can follow three pathways in its journey to the root vascular tissue for upward transport, namely, the apoplastic, symplastic, and transmembrane routes. The apoplast is the free diffusional space outside the plasma membrane, consisting of gaps between cells and the porous lattice network of cell walls, which serve as a filter to prevent soil and other large particles from entering the roots. The apoplastic route includes movement through these spaces, which does not include the crossing of any cellular membranes. In contrast, the symplastic route begins with P crossing a cell membrane into the cytoplasm where it moves cell to cell via connective channels between cells (plasmodesmata). Once a phosphate ion is inside the cell, it is possible to be transported between connected cells without crossing any additional membranes. However, the transmembrane route involves membrane transport between some cell and organelles, including across the vacuole membranes. This route results in the greatest control over which atoms and molecules are transported.

Although convenient to think of these as distinct and separate mechanisms of transport, these routes are connected and a phosphate molecule can be transported via any combination, even changing pathways at any time before reaching the endodermis. The half-time rate of exchange (t {1/2}) between external ions and the cytoplasm is between 23 and 115 min for phosphate, which is slower than for other ions (e.g., NH4 + is 7–14 min), but is orders of magnitude lower than exchange rates across the vacuole membrane (White, 2012a).

Water and low-molecular-weight solutes are typically the only compounds transported across membranes via the symplastic or transmembrane routes. Phosphorus exists in nature almost exclusively in its most highly oxidized form as phosphate. This form is taken up and utilized by plants. Phosphite (PO3 3−), a more reduced oxide of P, also can be taken up by plants, but it can be detrimental to plants that are already deficient in phosphate as it is an analog that inhibits phosphate uptake (Ratjen and Gerendás, 2009). The mono- and diprotonated phosphate ions (HPO4 2− and H2PO4 ) are the only significant forms of phosphate in a small enough molecular form to be transported across membranes, although plants can absorb certain soluble organic P forms, such as nucleic acids, in some cases.

However, slightly larger phosphate compounds can begin the journey into the plant by entering the apoplasm where it is theorized that conditions allow a protected environment for chemical transformations. For example, a phosphate ion cleaved from a phosphate ester has a high probability of forming a precipitate, such as calcium phosphate, if it dissociates in the unprotected bulk soil solution. If this reaction occurs, the precipitated P will not enter the plant unless it is resolubilized. Although the phosphate ester may be too large to cross cell membranes, it will enter the apoplasm. If it does so and then dissociates in this protected environment, it has a much higher probability of remaining soluble, due to the low pH and high organic acid concentration of the apoplasm. Once in the apoplasm, the orthophosphate has a much higher probability of being utilized by the plant.

Some phosphate ion molecules entering the root outer epidermal and cortical cells are utilized by these cells, but the vast majority is transported symplastically to and through the endodermis. The endodermis is an inner layer of cells in the root cortex surrounding the stele. Apoplastic movement is halted by the lipophilic Casparian strips of the cylinder of the endodermis, with connecting walls entrenched with suberin that minimizes apoplastic solute and solvent movement into the interior of the root. Atoms and molecules from the apoplasm must pass through the plasma membranes and protoplasts of the endodermal cells to reach the stele. It should be noted, however, that this endodermal seal is not perfect, as it is not fully developed at the root apex or when lateral root branches develop and temporarily sever the membrane system.

In nonsaline soils, the mineral ion salt concentration in the soil water is much lower than in the plant, and as such, an expenditure of energy is required for salt accumulation against a gradient in root cells. For example, although P concentration in soil solution is likely less than 0.050 mg L−1, the concentration in plant cells is thousandfold greater (at least 50–500 mg L−1). Active transport (requiring energy) across the root membranes is required to enable plants to accumulate some nutrients (and exclude other elements) at levels much higher than are in the soil. To facilitate active transport, the plasma membranes of epidermal, cortical, and endodermal cells contain various proton pumps that transport specific ions, including phosphate, against large concentration gradients. Some of these transporter proteins are selective for phosphate. Researchers are currently working on ways to increase the uptake of P, by stimulating these nutrient transport proteins in the root.

Once past the endodermis, phosphate ions are further transported across stele cells (through the same mechanisms previously described) to the vascular system, where they encounter pits that allow entrance into the xylem vessels or tracheids or are loaded actively into the xylem from the xylem parenchyma. At this point, they are able to be transported throughout the plant for essential uses. This soil–root system of P transportation is the dominant form of uptake in plants.

3.2.3  Absorption of Phosphorus by Shoots

Fertilizer is sometimes applied as a dilute foliar spray directly to leaves and stems or injected into irrigation water (fertigation). Unless the amount of irrigation water applied is very small, a majority of the fertigated P is washed into the soil for root uptake. However, a small amount of P deposited onto plant shoots can be absorbed internally. Foliar transport is similar to root transport, complete with the various transport mechanisms and phosphate transporters previously described.

Phosphorus application to leaves does result in P accumulation in the plant. However, it is important to realize that there are fundamental disadvantages for foliar absorption of P. First, P is washed easily or blown off leaves. Second, while roots have evolved to take in water, the water in a plant leaf is in the process of exiting via the transpirational stream and, therefore, foliar uptake of P requires it to diffuse against the transpirational stream or to pass through the cuticle of leaves. These actions occur, but are not as efficient as with root absorption. Also, there is a limit to the amount of salt that can be in contact with sensitive leaf tissues. Therefore, foliar P applications are not more efficient in supplying adequate P needs than soil applications, but P absorption can occur.

3.3  Physiological Responses of Plants to Phosphorus

Phosphorus is one of the essential elements required by all plants to complete their life cycles and without any substitute for its functions. The primary macronutrients, N, P, and K, are designated as such since they are most commonly deficient and not because of their concentration in plants. Although N and K almost always have the highest mineral nutrient concentrations, the secondary macronutrients [sulfur (S), Mg, and, especially, Ca] are often at higher or equivalent concentrations in plants as P.

Phosphorus is involved in every growth phase in every living cell. In agronomy and horticulture, P is vital in nutrient management for achieving maximum crop yields (Bennett, 1993; Bundy et al., 2005; Grant et al., 2001; Hopkins et al., 2008, 2010a,b,c, 2014; Marschner, 2012; Ozanne, 1980; Stark et al., 2004; Westermann, 2005; Young et al., 1985).

The central role of P in plants is in bioenergetics, as it is a component of the adenosine phosphates (ADP and ATP) used in photosynthesis to convert light energy to chemical energy and in respiration reactions. Therefore, all energy-requiring reactions in living organisms require P. In addition, P modifies enzyme activity in phosphorylation, activates proteins, regulates metabolic processes, and is involved in cell signaling and division (Dubetz and Bole, 1975). Furthermore, P is a structural component of nucleic acids, nucleotides, phospholipids, coenzymes, and phosphoproteins. When in monoester form, P is an essential ligand in enzymatic catalysis. Phytic acid, the hexaphosphate ester of myoinositol phosphate, is the primary P storage in seeds. Phosphates, inorganic or organic, also serve as cellular pH buffers. From a cellular perspective, P has widespread involvement in virtually every physiological process in plants.

The visual response when P is deficient is very different than for other nutrients—which are generally expressed in terms of decreased chlorophyll production (chlorosis). Rather, the development of dark green or purpling of leaves and stems is reported for P-deficient plants (Barben et al., 2010a,b,c, 2011; Bennett, 1993; Hecht-Buchholz, 1967; Hill et al., 2014a,b; Nichols et al., 2012; Summerhays et al., 2014). This darkening or purpling is due to the accumulation of photosynthates and anthocyanin, which are being inefficiently utilized due to reduced supply of chemical energy in the plant. Reduction in amount of chlorophyll, common to most other nutrient deficiencies, does not generally occur until advanced stages of deficiency and concentration, in fact, can increase (Rao and Terry, 1989) with the combination of slow growth and accumulation of these other compounds overcoming any development of chlorosis (Hecht-Buchholz, 1967).

(See color insert.) Phosphorus-deficient corn (

Figure 3.2   (See color insert.) Phosphorus-deficient corn (Zea mays L.) showing discoloration, chlorosis, and necrosis of leaves. (Photograph by A.V. Barker.)

It would be convenient if obvious visual symptoms were always apparent with plant P deficiency, but visual symptoms are the exception rather than the rule. The shoot purpling is frequently cited, especially for corn (Figure 3.2), as evidence of P deficiency; however, it is far more common to have a yield response to P fertilizer for crops without any purpling or other obvious visual symptoms. Most species are more likely to show a dark green color of leaves or shoots rather than purple or red (Figure 3.3). But these leaf coloration differences are rare, and the main visual symptom is less overall shoot growth with symptoms varying with plant species (Bingham, 1966; Hambridge, 1941; McMurtrey, 1948; Wallace, 1961). Although not generally easily discerned from a visual perspective, P-deficient plants show suppressions in leaf expansion (Fredeen et al., 1989) and number (Lynch et al., 1991). The zone of cell division is reduced in corn (Assuero et al., 2004). Reproductive tissues also are impacted by P deficiency due to delays in flower initiation, flower number, and seed formation (Barry and Miller, 1989; Bould and Parfitt, 1973; Rossiter, 1978). Also, root hydraulic conductivity is decreased due to a decrease in genes encoding aquaporins (Clarkson et al., 2000).

(See color insert.) Phosphorus-deficient cucumber (

Figure 3.3   (See color insert.) Phosphorus-deficient cucumber (Cucumis sativus L.) showing early necrosis of leaves. (Photograph by A.V. Barker.)

Root growth also can be restricted with P deficiency, but less so than shoots, resulting in an increase in the shoot/root ratio (Fredeen et al., 1989). Sucrose tends to accumulate in the roots of P-deficient plants in an apparent signaling of P deficiency. Additionally, the elongation rate of root cells may actually increase (Anuradha and Narayanan, 1991). In fact, Smith et al. (1990) found that in the legume and forage crop Caribbean stylo (Stylosanthes hamata Taub.), shoot growth decreased, but root growth continued due to P translocation to roots under P-deficient conditions. In some species, root clusters are common for plants growing on the most P-impoverished soils and enable these plants to mine the soil more effectively of P (Hawkesford et al., 2012).

Because plants are dependent upon root interception of P, deficiencies are relatively more common in the early part of the growing season when soils are cold or water logged and have small, slow-growing root systems unable to expand into the soil effectively. Ironically, the situation can be magnified with P deficiency if the situation is extreme enough to cause limited root growth or susceptibility to root and vascular tissue–damaging pathogens (Lambert et al., 2005; Westermann, 2005; Westermann and Kleinkopf, 1985), thus exacerbating the situation.

Potato (Solanum tuberosum L.) is arguably the crop species with the greatest susceptibility to P deficiency (Fixen and Bruulsema, 2014; Hopkins et al., 2014; Rosen et al., 2014). Hopkins et al. (2014) reviewed the impacts of P deficiency on potato roots and shoots (leaf size and growth of all plant parts), as well as tuber yield and quality (set, number, size, specific gravity, starch synthesis, maturity). Dyson and Watson (1971) reported that adequate P impacted leaf area index during the first 8 weeks after emergence resulting in a 17% increase in leaf area duration. Even though potato is very susceptible to P deficiency, like other plants, it rarely shows visual symptoms. In fact, it is much more common to have restricted yields with no readily apparent visual indications in the canopy other than slight stunting in some cases (Hopkins et al., 2014). When visual deficiency symptoms do occur (Figure 3.2), they appear as purpling in extreme circumstances (Barben et al., 2010a,b,c, 2011) but more commonly as a dark greening of the leaf tissue (Bennett, 1993; Marschner, 2012; Stark et al., 2003; Stark and Westermann, 2008). However, it is most common to have no evident color differences and only shortened internodes and, therefore, stunted shoots (Barben et al., 2010a,b,c, 2011; Bennett, 1993; Marschner, 2012; Nichols et al., 2012).

This situation, with extreme deficiency resulting in easily observable visual symptoms and the more common scenario with mild deficiency resulting in hidden hunger, is also true for other crops less sensitive to P deficiency than potato.

3.4  Genetics of Phosphorus Need and Acquisition By Plants

3.4.1  Genetic Control

A plant passes the necessary information for need and acquisition of P to its progeny in its DNA. The various needs and uptake properties of plants are controlled genetically, and there are variations of these inherited characteristics that can impact greatly plant P requirement and the ability to obtain the element. For example, P uptake capacity increases after P is withheld from plants and is correlated with an increase in the transcription of genes encoding proton-coupled P transporters (White and Hammond, 2008). This response is controlled by biochemical signals derived from the interplay between root and shoot P status (White, 2012a,b; White and Hammond, 2008). It is theorized that low-P root status initiates a complex regulatory cascade through a transcription factor and that increased transport of sucrose and microRNA in the phloem acts as a signal. It is known that there is a general response with high concentration of sucrose in phloem, an action that results in greater root biomass and upregulates the expression of genes encoding transporters for nitrate (NO3 ), PO4 3−, sulfate (SO4 2−), NH4 +, K+, and iron (Fe2+, Fe3+), but there are fine controls specific to P and controlled by shoot P concentration rather than in the roots (Drew and Saker, 1984; Drew et al., 1984; White, 2012a,b).

Drew and Saker (1984) and Drew et al. (1984) proposed a regulatory mechanism of excess P in shoots being transported back to roots to regulate P uptake. White (2012b) also states that production of specific microRNA compounds in shoots and their translocation to roots regulates the turning on or off of P deficiency response mechanisms. Resupply of adequate P shuts these mechanisms off, but not immediately, which is an important consideration for plants growing in nutrient solutions where P supply can change dramatically, resulting in P toxicity (Cogliatti and Clarkson, 1983). Furthermore, P deficiency decreases root hydraulic conductivity due to a decrease in genes encoding aquaporins (Clarkson et al., 2000).

White and Hammond (2008) stated that plant P status influences plant shoot/root biomass ratio, root morphology, P metabolism, and release of protons, phosphatases, and organic acids. All of these responses facilitate enhanced P uptake but are expressed differentially across and within species. Hawkesford et al. (2012) discuss the wide range of adaptive responses of plants to P deficiency (Lambers et al., 2006) triggered by P-starvation signaling pathways (Rolland et al., 2006).

Genetic differences for P need and acquisition across and within species are significant. Differences can be tied generally to microbial association efficiency, root exudates, and morphology and architecture of root systems (Pearson and Rengel, 1997), as well as P concentrations in plant tissues and total plant biomass. Not only are these differences scientifically interesting, but this knowledge can be exploited in the breeding and genetic alteration of crop plants to increase production and conserve mineral P fertilizer reserves. These differences are briefly discussed in the following, with examples from a few key species. Crop species are the primary focus because of their economic value and the use of fertilizer on them, and the degree of study is higher for these compared with most native species.

3.4.2  Differences Across Species

Cereal grain crops provide by far the most calories worldwide, with wheat being the leading crop for direct human consumption in developed countries and rice (Oryza sativa L.) in developing countries. Corn is the dominant species grown in the United States, with it and soybean (Glycine max Merr.) largely used for animal feedstuffs. Alfalfa (Medicago sativa L.) is also used widely as animal feed, especially in developed countries. Soybean is the leading oil crop in developed countries, followed by rapeseed (Brassica napus L.) and sunflower (Helianthus annuus L.). Soybean and palm (Elaeus spp. and Attalea maripa Mart.) are the leading oil crops in developing countries. Sugarcane (Saccharum officinarum L.) and sugar beet (Beta vulgaris L.) are the dominant sources of refined sugars. Potato is the predominant high-starch root and tuber crop in developed countries, with cassava (Manihot esculenta L.) followed closely by potato and sweet potato (Ipomoea batatas Lam.) as the main sources in developing countries. Although urban landscapes use fertilizers for some food production, the predominant land use is for functionality and aesthetics. Use of fertilizers in urban landscapes is significant, with turfgrass (combined across all species) being grown in all cities and towns and being the number one irrigated crop in the United States.

The vast majority of P fertilizer is applied on these species and, as such, most of the research with regard to P nutrition is focused on these species as well. There is a large focus on corn, which is moderately responsive to P fertilization, due to the sheer abundance of research data available on this key species. Many of the other crops behave similarly to corn, but some known differences are discussed below. Potato will also be a point of special emphasis because of its importance as an important world food crop and its very unique P nutrition needs. At the other end of the spectrum of P fertilization need are the turfgrasses, which rarely provide a response to P fertilization despite their intense cultivation.

The reason that there are large differences across and within species with regard to P need and acquisition efficiency is a complex interaction between genetic and phenotypic differences in tissue concentration, total biomass production, microbial interactions, and, especially, root morphology and architecture.

In general, plants that grow slowly are less likely to become P deficient than rapidly growing plants. Natively grown species in wildland areas, such as Cascade fir (Abies amabilis Douglas ex J. Forbes), typically are not fertilized and, as such, are adapted to surviving with the low quantities of naturally mineralized P that become available as rock minerals break down very slowly over time. In contrast, most crop species have been bred to grow rapidly to meet the tremendous demand for food, fuel, and fiber for more than seven billion people on this planet. As such, these plants have an enormous need for supplemental P to achieve high yields required by society.

Although crops generally have relatively high P uptake needs compared with natively grown plants, there are large differences across crop species as well. The difference for potato and corn has already been pointed out. Another example is with slow-growing perennials, such as a dwarf apple (Malus domestica Borkh.), having a relatively low P demand despite having a large canopy of leaves that have to be regrown each year. Other deciduous fruit species respond to P fertilizer infrequently even when soil P is low (Childers, 1966). This lack of response is partially due to the ability of these perennials to store P and translocate it to newly forming tissues. Also, the per day growth rate for these fruit trees, while faster than most noncrop native trees, is much slower than corn, for example.

Plants can be classified in terms of their PUE, which is the percentage of fertilizer or bioavailable soil P taken up by plants compared with the total applied and/or available in the soil. Plants with high PUE have a high P influx and/or a high root/shoot ratio (Föhse et al., 1988). Corn is an example of a modestly high P-use-efficient plant. Schenk et al. (1979) reported that corn employs a stress response by increasing the root/shoot ratio when P is limited, with some genotypes doubling the ratio when grown in low versus high P conditions. Baker et al. (1970) found that rooting depth and, to a lesser degree, P influx rate were the reason for corn hybrids having relatively high P efficiency. It seems that the most likely success for breeding for increased P efficiency in corn ought to be focused on increased root expansion in the soil rather than increased P uptake per unit of root length, although the latter may also be effective.

3.4.3  Potato Is an Inefficient Responder

In contrast to corn, potato is considered to be an inefficient responder when it comes to P fertilization (Miyasaka and Habte, 2001). Potato has a shallow, poorly effective root system, especially with regard to P uptake (Asfary et al., 1983; Lesczynski and Tanner, 1976; Love et al., 2003; Munoz et al., 2005; Opena and Porter, 1999; Pack et al., 2006; Pan et al., 1998; Peralta and Stockle, 2002; Pursglove and Sanders, 1981; Sattelmacher et al., 1990; Tanner et al., 1982; Yamaguchi and Tanaka 1990). Weaver (1926) studied the root architecture and density of several major crops and found potato roots to be less dense, less branched, and shallower than all of the others. Tanner et al. (1982) found that a majority of potato roots reside in the top 60 cm of soil, with 90% of root length in the top 25 cm, whereas most other crops root more deeply. Lesczynski and Tanner (1976), Yamaguchi and Tanaka (1990), and Iwama (2008) had similar findings, with potato having the lowest root density by a substantial amount than the other five major crop species compared. For example, the root density for wheat was fourfold greater than potato.

In addition, potato has fewer root hairs than most other crops. Dechassa et al. (2003) found that potato and carrot (Daucus carota L.) yielded only 16% and 4%, respectively, of maximum when grown under very low P condition, in contrast to cabbage (Brassica oleracea var capitata L.) at 80%. Potato and carrot had a very low root to shoot ratio and, more importantly, low P influx rates due to a low number of root hairs. When soil P supply is low, the expanded reach of root hairs contributes up to 90% of total P uptake (Föhse et al., 1991). Potato has a relatively high total root length density, about the same as more P-efficient cotton (Gossypium hirsutum L.), sugar beet, and many vegetables. However, it has 50% less total root length density than winter wheat and oilseed rape (Stalham and Allen, 2001). However, the main reason for its poor P efficiency is attributed to root hairs comprising only about 21% of the total root mass, compared with 30%–60% for most other crop species (Yamaguchi, 2002).

Furthermore, the root system for potato tends to decline in the late season when P demand is at its highest, a response that is in contrast to many other species that accumulate P relatively earlier in the growing season (Fixen and Bruulsema, 2014). However, Jacob et al. (1949) observed that potato takes up a greater proportion of P later in the growing season compared with other crops. Furthermore, potato P continues to be taken up later in the growing cycle than is either N or K (Carpenter, 1963; Kleinkopf et al., 1981; Lorenz, 1947; Roberts et al., 1991; Soltanpour, 1969). Phosphorus uptake progresses steadily throughout the season, whereas N shows little if any additional uptake after about 80 days after emergence (Kelling et al., 1998). This situation is a significant disadvantage for potato, especially in light of its susceptibility to pathogens that may degrade the root and vascular systems, negatively impacting the uptake and translocation of P. Thornton et al. (2014) suggest that it is likely that PUE in potato could be improved by breeding for more extensive root systems and increased root hair production. They cite Deguchi et al. (2011) already using this approach to breed potato cultivars with improved drought resistance due to better water uptake efficiency, which also likely improves P uptake.

As a result of these and possibly other genetic differences, fertilizer recommendations and soil test cutoff levels for potato are globally much higher than for other crops (Fixen and Bruulsema, 2014; Hopkins et al., 2014; Kelling and Speth, 1997; Lang et al., 1999; Moorhead et al., 1998; Rosen et al., 2014). Fertilizer rates can be higher than 400 kg P2O5 ha−1 in long-season, high-yielding environments. A survey of state university research–based fertilizer recommendations shows that most other crop species require about half the amount of P that potato requires. For example, in the United States, a large majority of potato production occurs in the Pacific Northwest states. In these states, the maximum recommended fertilizer rate is 134 kg P2O5 ha−1 for corn (Brown et al., 2010), whereas the maximum rate for potato ranges from 252 to 493 kg P2O5 ha−1 (Lang et al., 1999; Stark et al., 2004). Similarly, the University of Wisconsin recommends optimum levels for soil test P (Bray P1) at, depending upon soil texture and so forth, between 16 and 50 mg kg−1 for various crops except potato, which has optimum test levels of 61–200 mg kg−1 (Laboski and Peters, 2012). Truly, potato has unique genetic differences from most other species that need to be examined.

3.4.4  Unique Differences for Phosphorus Uptake across Species

Fast-growing, short-season vegetable crops are often similar to potato in their relatively high P need, although not generally as extreme (Alt, 1987; Greenwood et al., 1980; Itoh and Barber, 1983; Nishomoto et al., 1977; Sanchez, 1990).

A contrasting species with regard to P nutrition is sugar beet. Its root architecture and morphology are vastly different to most other species, sending a taproot largely downward for the first several weeks of growth in an effort to ensure adequate water supply. The negative by-product of this root growth strategy is that the nutrient-rich topsoil is left largely unexplored for several weeks. As a result, yield deficiencies due to early-season P deficiencies caused by the development of fewer and thinner cambial rings are common.

Alfalfa is also a taprooted species, but it has more balanced growth early in its establishment and is very efficient at surface soil feeding and thus is less impacted by P deficiencies at establishment. However, this species is grown as a perennial and is unique in that large amounts of P are removed through the harvested hay over time. As such, alfalfa is very responsive to P fertilizers when grown in soil with low to moderate soil test P levels—especially after years of P removal through crop harvest. The challenge for this and many other perennials is that P can be surface applied only after initial establishment. Fortunately, its surface-feeding rooting efficiency enables this approach when other species are less adept at P recovery from broadcast applications of fertilizer not incorporated into the soil.

Soybean is another major world crop, but it is somewhat unique in terms of P need. Soybean has much less total biomass production than corn and, thus, less total P uptake. Its root system is relatively shallow and less extensive than corn and most other crops, but it is efficient at P recovery in soil due to a majority of its roots being in the P-rich topsoil. In the United States, it is common to grow soybean in rotation with corn, with growers often not applying any supplemental P fertilizer to the soybean crop directly, allowing the plant to feed off of the remnants of the corn crop. Wheat and rice and most other grains approach corn in terms of their P fertilization needs but take up less total P as a function of relatively lower biomass yield.

Although similar to corn in biomass production and canopy architecture, sorghum (Sorghum bicolor Moench) thrives in relatively less fertile soils with less fertilizer application, due to its extremely fibrous and extensive root system. Sorghum roots effectively explore a larger volume of soil than most other crop plants due to this fibrous root system. Cassava is similar to sorghum in terms of its ability to thrive in less fertile soil, which enables it to be successfully grown in regions where fertilizers are not readily available or affordable to indigenous populations.

Like sorghum, turfgrass species also have very fibrous and efficient root systems. However, they differ in terms of much lower biomass production. Additionally, turfgrasses tend to root only in the top few cm of the P-rich topsoil. These factors result in very little need for P fertilization. In fact, turfgrass species grown in soil with modestly low residual P levels often have a competitive edge over invasive weeds. Although not typically managed for any type of biomass production, turfgrass species are among the most intensively cultivated plants, often with removal of mowing clippings multiple times in a week, and yet they can often go without P fertilization for many years without suppression in growth. As long as bioavailable P is not extremely low, established turf can often go for several years without supplementary P fertilization (especially if clippings are returned to the soil during mowing). The exception would be newly seeded/sodded fields and sports fields where frequent seeding and sodding are performed. These situations have plants without extensive root systems, and the P need during establishment is relatively higher than when maturity is reached and their root systems are well established.

3.4.5  Differences Within Species

Differences in P efficiency are not only observed across species, but also within. Schenk et al. (1979) evaluated five corn genotypes, and although all increased the root/shoot ratio under P-deficient conditions, the magnitude of difference was significant. Buso and Bliss (71) showed differences across lettuce (Lactuca sativa L.) varieties, although others found little difference (Nagata et al., 1992; Sanchez and El-Hout, 1995).

Varietal differences for potato yield response to P have been measured (Freeman et al., 1998; Jenkins and Ali, 1999; Moorhead et al., 1998; Murphy et al., 1967; Sanderson et al., 2002, 2003; Thorton et al., 2008). Thornton et al. (2014) report that the Shepody cultivar has greater root density and earlier maturity, which both contribute to its being less responsive to P than the widely grown Russet Burbank cultivar. Thornton et al. (2014) report differences among potato varieties in terms of PUE. The recently released Alturas cultivar has an even greater efficiency with much lower fertilizer P requirement than other cultivated varieties due to its more extensive and efficient root system. McCollum (1978a,b) reported similar findings with “Ranger Russet” and “Premier Russet” reaching maximum yield at a lower level of P fertilization than “Shepody” or “Russet Burbank.”

Potato cultivars differ in total root length density and depth of soil penetration due mostly to differences in the time of active root growth and development (Stalham and Allen, 2001). For example, the duration of root growth was almost half (Olsen et al., 1954) for “Cara” compared to “Atlantic” (Wagganman, 1969). The longer the time of active root growth, the deeper and more soil explored. Iwama et al. (1981) found a wide difference in 268 unselected clones from 1.3 g root dry weight plant−1 to 2.8 g for early versus late maturing clones, respectively.

Another difference common within species is related to pathogen susceptibility, which can have a large impact on P status in plants (Lambert et al., 2005). Pathogens that attack and degrade root tissue limit the ability of the plant to encounter P, and pathogens that infect vascular tissues result in inability of plants to move P from roots to shoots and vice versa. As such, varietal differences in disease susceptibility can have a major impact on P nutrition.

For example, potato is highly susceptible to root and vascular system pathogens, a trait that is partly the explanation of why this species is unique with respect to its P need (Rosen et al., 2014; Thornton et al., 2014). Phosphorus deficiency can increase the severity of several important potato diseases, including common scab (Streptomyces scabies), Verticillium wilt (Verticillium dahliae and Verticillium albo-atrum), and late blight (Phytophthora infestans). Davis et al. (1994) showed a close relationship between P fertilizer rate, wilt symptoms due to V. dahliae, and pathogen colonization of stem tissue. As optimal or higher levels of P can speed tuber maturity and increase skin thickness, Herlihy and Carroll (1969) and Herlihy (1970) found that P reduced tuber infection with late blight. As previously mentioned, P uptake occurs relatively late for potato and yet root system development ceases 60–90 days after planting and, in fact, the roots actually begin to deteriorate at this time. Furthermore, these developments all coincide with when disease development hastens rapidly while tubers are bulking rapidly and nutrient requirements are still high (Pan et al., 1998; Thornton et al., 2014). Although these principles are generally true for potato, there is a very wide difference in disease susceptibility by cultivar. The most commonly grown cultivar is “Russet Burbank,” but it is also very susceptible to disease and has a very high P fertilization requirement compared with improved varieties.

Although these interactions between nutrition and pathology are more relevant for the highly susceptible potato compared with most other species, it is important to realize that P deficiency may make a plant more susceptible to pathogen infection, and diseases that degrade root or vascular tissue can impair P uptake even when soil P levels are high.

3.4.6  Genetic Modification Potential

As fertilization and other agricultural improvements led to the Green Revolution, the next revolution is advanced genetic modification potential. Thornton et al. (2014) state that both quantitative trait locus (QTL) mapping and marker-assisted selection have been identified as useful tools to facilitate breeding for complex traits such as PUE. The QTL associated with enhanced P uptake has been identified in several species, such as pearl millet (Pennisetum glaucum R. Br.), corn, and rice (Hash et al., 2002), but little work has been done in species such as potato. However, Thornton et al. (2014) state that recent research aimed at improving drought resistance has identified QTLs associated with root length and root dry weight on chromosome 5 in potato (Iwasa et al., 2011). This same approach could be used to improve identify root traits or other characteristics associated with improved PUE.

Another avenue is genetic modification by impacting direct P acquisition or other cellular mechanisms. Miyasaka and Habte (2001) identified the genes for high-affinity P transporters in arabidopsis (Arabidopsis thaliana Heynh.), shown to increase P uptake at low P concentrations by almost threefold. Advances in breeding disease resistance also have large potential to have a secondary impact on P nutrition. Breeders, pathologists, and agronomists will need to work together to provide a better understanding of how disease resistance and control practices impact root health as a way to improve P uptake efficiency throughout the growing season (Thornton et al., 2014). There is significant opportunity for the genetic improvement of PUE in crop plants (Lynch, 1998).

Lambers et al. (2011) suggest that the genetics of native species growth on severely P-deficient soils be explored as an avenue to enhance PUE. One approach that has been suggested by Thornton et al. (2014) to improve PUE in potato is to take advantage of native germplasm from South America. These native plants have evolved under conditions of low soil nutrient availability and may, therefore, have more efficient and extensive root systems. However, Sattlemacher et al. (1990) evaluated 27 native clones and 9 advanced cultivars under conditions of low and high soil nutrient availability and concluded that the advanced group had higher yield potential under both scenarios, and showed no evidence of having reduced nutrient-use efficiency compared with the native group. Nevertheless, the native germplasm should be explored for potential crosses, which may result in improved varieties.

3.5  Concentrations of Phosphorus in Plants

Mineral nutrients generally make up less than 10% of the dry weight of a plant, with N and K generally at ~2%–5% each followed by similar concentrations of P, Ca, S, Mg, and chloride (Cl) at 0.1%–1% each. The micronutrients, other than Cl, are at concentrations several orders of magnitude lower than the macronutrients. Mills and Jones (1996) have published typical P concentrations for a wide variety of aboveground plant parts ranging from 0.08% to 1.3%, although it is possible to have slightly lower levels with roots sometimes down to levels of 0.04% but in some reports as high as 4% (Hawkesford et al., 2012). Typical P levels in plant tissue are shown in Table 3.1, ranging from the very-slow-growing, native Cascade fir with very low P levels in its tissues to the high levels of P in coleus (Coleus spp. Lour. now largely Plectranthus spp. L’Hér).

Lambers et al. (2010) stated that the P requirement for optimal growth is 0.3%–0.5% but that some plants evolving on P-limiting soils may contain an order of magnitude less. The chance of P toxicity increases at levels above 1%, although this is rare because plants downregulate their P transporters when P levels are high (Dong et al., 1999). However, toxicities do occur in unique circumstances (Hawkesford et al., 2012; Shane et al., 2004). Hawkesford et al. (2012) point out the wide variety of tolerance to levels of P, with toxicity identified in pigeon pea (Cajanus cajan Millsp.) and black gram (Vigna mungo Hepper) at levels as low as 0.3% and 0.6% shoot P, respectively, while the very-fast-growing green mulla mulla (Ptilotus polystachyus F. Muell.) shows no signs of toxicity at 4% shoot P.

Table 3.1   Average Phosphorus Plant Tissue Concentrations

Species

Plant Part

Timing

P, %

Alfalfa (M. sativa L.)

Whole tops

Prior to flowering

0.26–0.70

Apple (M. domestica Borkh.)

Mature new leaves

Summer

0.09–0.40

Cascade fir (A. amabilis Doug. ex J. Forbes)

Terminal cuttings

Summer

0.09–0.16

Coleus (Plectranthus spp.)

Mature new leaves

Mature plants

1.1–1.3

Cotton (G. hirsutum L.)

Petioles

First squares to initial bloom

0.30–0.50

Petioles

Full bloom

0.25–0.45

Corn (Z. mays L.)

Whole tops

<30 cm tall

0.30–0.50

Leaves below whorl

Prior to tasseling

0.25–0.45

Ear leaves

Initial silk

0.25–0.50

Rapeseed (B. napus L.)

Leaves, 5th from top

Rosette to pod

0.28–0.69

Rice (O. sativa L.)

Mature new leaves

Maximum tillering

0.10–0.18

Sorghum (Sorghum vulgare Moench)

Whole tops

23–39 days after planting

0.30–0.60

Mature new leaves

37–56 days after planting

0.13–0.25

Third leaf below head

Bloom

0.23–0.35

Third leaf below head

Grain in dough stage

0.15–0.25

Soybean (G. max Merr.)

Mature new leaves

Prior to pod set

0.25–0.50

Sugar beet (B. vulgaris L.)

Mature new leaves

80 days after planting

0.45–1.1

Source: Based upon Mills, H.A. and Jones, J.B., Plant Analysis Handbook II, MicroMacro Publishing Inc., Athens, GA, 1996.

Fractions of phosphorus occurring in plants.

Figure 3.4   Fractions of phosphorus occurring in plants.

Bieleski (1973) states that a typical plant contains the fractions as shown in Figure 3.4. There is not a similar comprehensive listing of P concentrations in root tissues. Separating roots from soil is difficult. As a result, P concentrations in roots generally are not measured commercially and rarely are reported in the scientific literature. In general, P concentrations measured across a wide variety of species at the Brigham Young University Environmental Analytical Lab shows that P concentrations in shoots are ~25%–200% higher than in root tissue. In addition, it is difficult to quantitatively gather all of the roots from a plant growing in soil. Therefore, total root uptake of P is rarely measured or reported. However, we know that root biomass is generally much less than shoot biomass, with ratios ranging from 0.10 to 0.3. The combination of lower biomass and lower P concentration results in only a small amount of the total P being in roots.

Succulent new tissues (either roots or shoots) tend to be higher in P than in lignified stems and other older tissues. Even in nonwoody crop tissues, the P concentration will drop dramatically in just a few weeks, as shown for cotton, corn, and sorghum in Table 3.1 and for potato in Figure 3.5. Phosphorus is highly mobile within the plant, with much of it being cannibalized from senescing tissue to newer growth and reproductive organs as the season progresses. Plants mobilize P and some other nutrients to seeds, tubers, and other reproductive tissues to provide ample nutrition for the next cycle of growth. When these tissues are harvested, a significant quantity of P is removed from the soil (Table 3.2).

Average seasonal potato (

Figure 3.5   Average seasonal potato (S. tuberosum L.) petiole phosphorus concentrations for unfertilized ‚óŹ and fertilized ♦ (150 kg P2O5 ha−1) plots with Olsen bicarbonate P concentration of 23 mg kg−1 prior to fertilization.

Table 3.2   Uptake into Aboveground Biomass and Crop Removal for Phosphorus at Average Yields

Crop

P Uptake Rate, kg Mg−1

Removal Rate, kg Mg−1

Average Yield, Mg ha−1

Total P Removal, kg ha−1

Alfalfa (M. sativa L.)

5.7

6.0

7.2

43

Corn (Z. mays L.), grain

9.6

6.3

10.0

63

Silage

9.6

1.6

42.0

67

Potato (S. tuberosum L.)

2.1

1.5

47.0

70

Rice (O. sativa L.)

8.4

6.7

8.6

58

Sorghum (S. vulgare Moench), grain

13.0

7.8

3.8

29

Soybean (G. max Merr.)

18.0

12.0

2.9

35

Sugar beet (B. vulgaris L.)

1.4

1.1

64.0

70

Wheat (Triticum aestivum L.) spring

13.0

9.5

3.2

30

Winter

11.0

8.0

3.2

25

Source: Based on Mills, H.A. and Jones, J.B. Jr., Plant Analysis Handbook II, Athens, GA: MicroMacro Publishing Inc., 1996; USDA, Crop production 2013 summary. National Agricultural Statistics Service, 2014. http://www.usda.gov/nass/PUBS/TODAYRPT/crop1014.pdf. Accessed July 21, 2014.

It is noteworthy that the values in Table 3.2 are only averages and, in some cases, the removal rates are substantially higher. For example, irrigated wheat yields in the Pacific Northwest have approximately threefold higher yields than the average shown, and potato yields are double the national average in the Columbia Basin in Oregon and Washington due to a large number of growing degree days and otherwise optimal conditions. Removal rates for nutrients would be proportionally higher based on actual yield removal. Understanding and managing depletion rates are important factors when developing a sustainable plan for crop production, although basing fertilizer recommendations solely on these values is not recommended as in many cases much higher rates are needed or, in other cases, it being appropriate to harvest excess P from soils with excessive levels.

3.6  Ratios of Phosphorus With Other Elements and Interactions

3.6.1  General Interactions between Phosphorus and Other Nutrients

Interactions among nutrients in soil or other growth media can impact plant health, yield, and nutrient concentrations and ratios (Fageria, 2001; Foy et al., 1978; Reichman, 2002). Nutrient interactions with P are widespread and important. In general, the physiological effects of P on plants impact other nutrients. For instance, P deficiency results in restriction of shoot growth, whereas root growth often remains the same or is even increased. This result can lead to an accumulation of nutrients in shoots due to greater root contact per unit of shoot growth. However, under extreme P deficiency, a lack of energy supply can result in limited active uptake of nutrients, such as K. Other general interactions include overall plant health degradation with any nutrient deficiency or toxicity resulting in reduced root growth, increased pathogen infection, and reduced ability to actively take up nutrients.

A beneficial interaction occurs if P is applied in conjunction with NH4 +–N. This interaction appears to enhance the plant uptake of both nutrients due to increased P solubility, increased shoot and root growth, and alteration of plant metabolism (Bundy et al., 2005; Engelstad and Teramn, 1980; Leikam et al., 1983; Murphy et al., 1978). These observed benefits are more likely to occur for plants growing in soil with minimal bioavailable P (Engelstad and Teramn, 1980). However, excess N availability can result in decreased shoot-to-root ratios more so than any other nutrient excess, causing P supply issues.

Chloride in close proximity with phosphate also has been shown to restrict P uptake (Berger et al., 1961; Hang, 1993; Kalifa et al., 2000; Zhong, 1993). Reducing the Cl content of band-applied K helps avoid this problem (Berger et al., 1961), although Panique et al. (1997) saw no decrease in P uptake even where 448 kg K2O as KCl ha −1 was banded near the row. James et al. (1970) also noted no effect of Cl on P uptake. There is also speculation of competitive antagonism with other anions, such as NO3 , SO4 2−, borate (BO3 3−), and molybdate (MoO4 2−), although the evidence for competitive antagonism is sparse and conflicting, and field data do not seem to support it.

However, P has a well-documented antagonistic interaction with Ca and Mg in soil due to chemical bonding with P, for which precipitates are not very soluble, especially in alkaline soils. These precipitates can also occur within roots and other plant tissues, but the acidic biological environment allows for solubilization more readily than with soil. Similarly, aluminum (Al), manganese (Mn), Fe, Zn, and copper (Cu) can precipitate with P in soil. These precipitates can form under alkaline conditions, but Al, Mn, and Fe phosphates are known to precipitate under strongly acidic conditions. In the case of Al, this element solubilizes at about pH 5.5 and below. Once in soil solution, Al can precipitate with P. A similar reaction occurs with Mn and Fe. The interaction between P and the various metals, which occurs in plants and soils, is one of the more well-known and studied interactions.

3.6.2  Phosphorus–Micronutrient Metal Interactions

The P–Zn interaction is the most documented and well known. Boawn et al. (1963) reported Zn deficiency as a result of high P fertilization levels. The P–Zn antagonism was documented in subsequent works (Boawn and Leggett, 1964; Jackson and Carter, 1976; Soltanpour, 1969). Broadley et al. (2012) discuss the interaction of P–Zn and offer several possible explanations for this antagonistic interaction when high rates of P fertilizer are applied to plants, including (1) decrease of Zn solubility in soil, (2) reduced root growth, (3) reduced arbuscular mycorrhizal colonization, (4) dilution effect due to higher yields, (5) reduction of Zn solubility and mobility in plant tissues, and (6) P toxicity. Barben et al. (2011) found that increasing available Zn generally reduced shoot P and increased root P in potato. This effect of solution Zn was exacerbated by optimal and excessive solution P, an occurrence that is similar to observations in other studies (Barben et al., 2010a; Boawn and Leggett, 1964; Chatterjee and Khurana, 2007). This action was likely due to a P–Zn binding in roots, as was suggested in other research (Leece, 1978; Singh et al., 1988; Terman et al., 1972).

Barben et al. (2011) thoroughly reviewed the complex interactions between P, Zn, Mn, Fe, and Cu. Their data show a strong three-way interaction between P, Zn, and Mn levels that also can impact concentrations of Fe and Cu. Their data mostly support other findings of an antagonistic interaction between Zn and P that has been observed commonly and studied and that can result in excessive P uptake under Zn deficiency (Barben et al., 2010a,b; Bingham, 1963; Boawn and Leggett, 1964; Loneragan et al., 1979; Webb and Loneragan, 1988) or in a P-induced Zn deficiency (Christensen, 1972; Christensen and Jackson, 1981; Soltanpour, 1969). Apparent in the Barben et al. (2011) study, but inconsistent with some previous studies (Barben et al., 2010a,b; Bingham and Leggett, 1963; Boawn and Leggett, 1964; Cakmak and Marschner, 1987), shoot Zn was reduced at excessive solution P relative to deficient or optimal solution P, regardless of Mn level. These findings support reduced shoot Zn with high available P in potato as suggested by others (Christensen, 1972; Christensen and Jackson, 1981; Soltanpour, 1969).

Although the P–Zn interaction is studied most commonly, other cationic micronutrients such as Mn, Fe, and Cu interact with P as well (Barben et al., 2011; Beer et al., 1972; Brown and Tiffin, 1962; James et al., 1995; Safaya, 1976). Phosphorus and Mn interactions have been reported in several species (Barben et al., 2010a,b; Ducic and Polle, 2007; Gunes et al., 1998; Le Mare, 1977; Marsh et al., 1989; Neilsen et al., 1992; Nogueira et al., 2004; Rhue et al., 1981; Sarkar et al., 2004; Sharma and Arora, 1987; Zhu et al., 2002). Reductions in plant P with increasing Mn were observed in tomato (Solanum lycopersicum L.; Gunes et al., 1998) and potato (Sarkar et al., 2004), whereas a rise in P was seen in shoots and roots of sorghum with increasing Mn (Galvez et al., 1989). Barben et al. (2010c) found that when Zn availability was held constant as Mn varied, plant P consistently was depressed, especially in shoots, at optimal solution Mn compared to either deficient or excessive available solution Mn.

Although Zn has a larger impact on plant Cu, P influences depressed Cu levels as well (Forsee and Allison, 1944; Halder and Mandal, 1981). Safaya (1976) reported that a strong P x Zn interaction also affects total Cu uptake. Other studies show that the effects of Zn on Fe uptake and transport in plants do not result only from increasing available Zn, but are also strongly influenced by P x Zn (Hamblin et al., 2003). While most studies agree that reduced shoot Fe results from Mn interference with Fe translocation, root interactions also influence reductions in Fe with some studies suggesting Mn-induced P–Fe binding within roots (Alvarez-Tinault et al., 1980; Cumbus et al., 1977).

Precipitation in roots of micronutrient-bound PO4 3− is indicated by several studies (Leece, 1978; Singh et al., 1988; Terman et al., 1972) and likely explains the results of Barben et al. (2011) with high available P. At low available P, however, little explanation has been given. Reduced nutrient transport from root to shoot due to unavailable compounds involved in P metabolism (e.g., ATP, ATPases, alkaline phosphatase, and phosphoenolpyruvate carboxylase), which are required to provide the necessary energy for nutrient mobilization via proton pumps and other mechanisms in transmembrane transport (Clemens et al., 2002; Fox and Guerinot, 1998; Grusak et al., 1999), and as such, is a reasonable explanation.

3.6.3  Management of Interactions

It is apparent that nutrient interactions occur in the soil and in plant tissues. The next logical step may seem to manage nutrients based on ratios of P with other nutrients. However, the empirical evidence raises a flag of caution for this approach. It is not uncommon for soils and crops to be analyzed for management purposes, with many laboratories printing various ratios on these reports. Whether intended or not, these ratios imply that there is an ideal ratio to achieve maximum production efficiency. This approach, while appearing to be logical, is not supported generally by field research. There are exceptions of course, such as with the sodium absorption ratio (SAR) for soil and irrigation water analysis, which have been shown by research and field application to be useful values in managing sodium (Na)-affected conditions (Hopkins et al., 2007b). However, there is no such conclusively proven ratio for P with any other element.

Table 3.3 shows the approximate ratio of all of the essential elements, as compared with P, in plant tissues. Although this information is interesting, it should not be used as a management tool in an attempt to fertilize to achieve a certain ratio of P with any other nutrient. This approach might be especially tempting for the P and Zn interaction outlined earlier, which has been well documented and studied. For example, according to the sufficiency range suggested by Mills and Jones (1996) for corn at the initial silk stage, the concentration ranges are 2500–5000 and 20–60 mg kg −1 for P and Zn, respectively. Assuming the widest ratios within these ranges would be acceptable, the ideal P:Zn ratio could be assumed to be from 50 to 250 times as much P as Zn. However, an informal survey of dozens of unresponsive corn P and Zn trials (Hopkins, unpublished data) shows above-average yields in many of these trials where this supposed ideal ratio is violated. For example, in one trial, the extremely high P fertilizer rates resulted in leaf concentrations of 21 and 7200 mg kg −1 for Zn and P, respectively, a ratio of 348 times more P than Zn. The yields of this treatment were 17.5 Mg ha −1 , which is nearly double the national average and similar to the others with less P fertilizer and resulting in more normal P concentrations. Obviously, the wide ratio did not impact yield. One could argue that this event is an anomaly, but many such instances occur in growers’ fields and in field research. More importantly, no strong research evidence shows a good correlation between tissue P:Zn ratios and yield. Despite this fact, it is somewhat commonplace for field managers and tissue-testing services to recommend fertilizer based on these ratios.

Table 3.3   Average Ratio on a Mass Basis of Nutrients Relative to Phosphorus

Nonmineral

Plant Shoots

Carbon

C

210

Oxygen

O

210

Hydrogen

H

25

Mineral

Primary macronutrients

Nitrogen

N

15

Potassium

K

10

Secondary macronutrients

Calcium

Ca

4.5

Sulfur

S

0.75

Magnesium

Mg

0.75

Micronutrients

Chloride

Cl

0.5

Iron

Fe

0.25

Manganese

Mn

0.025

Zinc

Zn

0.015

Copper

Cu

0.0025

Boron

B

0.0025

Molybdenum

Mo

0.0001

Nickel

Ni

0.00025

Note: Based on compilation of a wide variety of mostly crop plants from data at the Brigham Young University Environmental Analytical Lab and Hopkins research data sets.

Even more common are fertilizer recommendations made based on some ideal soil test ratios. Soils vary much more widely in terms of total and bioavailable ratios as compared with plant tissue concentrations. Elements that typically have much higher total and bioavailable elemental concentrations in soil than P include C, O, H, N, K, Ca, Mg, and Na. Aluminum, silicon (Si), and Fe typically have higher total concentrations than P in soil, but generally have lower bioavailable levels. Nutrients other than those listed earlier are typically equal to or, for most, much lower than total or bioavailable P, although there are many exceptions (such as the S in a soil with high concentrations of gypsum). Although these general trends exist, the ratios of P to other elements in soil vary widely.

Those who promote ideal soil test ratios forget that plants largely self-regulate uptake and exclusion of many elements. Just one example is Ca and P. Calcium typically is found at concentrations much higher than P in soil, and yet plants actively take up P and exclude some Ca so that levels in most plant species are close to equivalent for these nutrients. When comparing ratios, Ca is many-fold higher than P in high base saturation and calcareous soils, giving a very high Ca to P ratio. Although it is true that Ca levels are higher in plants in these circumstances, they do not follow the same proportions as what is found in the soil. Managing by some supposed ideal ratio would not be practical. Rather, P should be managed by bioavailable P concentration, and in some cases, the recommendation needs to be modified based on concentration of Ca minerals (Westermann, 1992), but not on some fictitious ideal ratio.

Another example of a ratio that would possibly be important would be P:Zn, but no strong evidence can be found to support such a claim. In fact, an informal survey from the files of a large crop-consulting corporation in the Midwestern United States (Servi-Tech Inc., Dodge City, Kansas, United States) shows that in fields with above-average yields, these yields were not correlated to the P:Zn soil test ratio. The only facts that have been shown in the P–Zn research cited earlier is that very high rates of P fertilizer can induce micronutrient deficiencies and vice versa. These studies were all based on added P fertilizer and not on existing high soil test levels. Therefore, P and micronutrients need to be managed according to their individual soil test values and experimentally derived information on crop need, with appropriate levels of fertilizer added without excess. In other words, P fertilizer should not be added to a soil just because the soil test Zn, Mn, Fe, or Cu levels are exceptionally high or vice versa. These nutrients are managed on their individual concentration levels and not according to ratios of one to another.

3.6.4  Differences across and within Species

Table 3.3 shows a ratio of average plant tissue concentrations. It is vital to understand that these ratios vary widely across species. For example, typical concentrations for P are similar for corn and alfalfa at about 0.25%–0.6%, but Ca is drastically different, with corn having Ca concentrations in the same range as P, but alfalfa typically having Ca at 1.8%–3.0% in its shoots (Mills and Jones, 1996). This difference in P:Ca ratio of about 1:1 for corn and 1:5 for alfalfa shows that ratios can vary widely across species.

Within species, differences are also significant. The temporal nutrient concentration differences that occur through the course of a growing season and differences across varieties/cultivars/ hybrids were discussed previously. These differences are not surprising, but it is also important to note that there can be significant phenotypic differences even within the same genotype based on soil and environmental conditions. For example, Table 3.4 shows the results of selected sugar beet trials in Idaho, where the unfertilized treatments had similar sugar yields and quality compared with those fertilized with P. All of the fields had the same variety, and the fields selected had good fertility and management, with the result of above-average yields. These data show that high yields are obtained, and yet the petiole P concentrations vary widely (note that all of these values are above the established critical level). The K concentrations for these fields also are shown, along with the ratio of P to K, showing a very wide range to illustrate that it is unlikely there is some ideal P:K ratio to be achieved in order to obtain high yields. This example is just one, but a survey of farm field results and research publications shows a wide variety in the ratios of essential nutrients, with no strong correlation between some supposed ideal optimum ratio and yield parameters.

Table 3.4   Concentration of Phosphorus and Potassium and K:P Ratios in Sugar Beet (B. vulgaris L.) Leaves from 11 Field Samples

Field

P, %

K, %

K:P

1

0.45

3.6

8.0

2

0.55

4.3

7.8

3

0.67

6.0

8.9

4

0.56

2.1

3.7

5

0.87

4.1

4.7

6

0.54

5.2

9.7

7

0.98

4.7

4.8

8

1.07

2.5

2.3

9

0.56

5.7

10.0

10

0.46

4.3

9.3

11

0.49

3.2

6.4

3.7  Diagnosis of Phosphorus Status in Plants

Determining whether there is sufficient P available to plants is possible through tissue analysis as a function of critical values and sufficiency ranges (Macy, 1936). These acceptable ranges are typically determined by plotting yields relative to plants having adequate P (yield = 100%) against P concentration in plant tissue (Figures 3.6 and 3.7). Often, the critical level is set at 90% or 95% of maximum for most crops and 98% or 100% for higher-value crops (based on the principle of maximum economic yield).

Critical concentration using a curvilinear model of phosphorus in midribs of endive (

Figure 3.6   Critical concentration using a curvilinear model of phosphorus in midribs of endive (Cichorium endivia L.) at the eight-leaf stage. (From Sanchez, C.A., Phosphorus, in Handbook of Plant Nutrition, Barker, A.V. and Pilbeam, D.J. (eds.), CRC Press, Boca Raton, FL, 2007, pp. 51–90.)

Critical concentration using a linear and plateau model of phosphorus in radish (

Figure 3.7   Critical concentration using a linear and plateau model of phosphorus in radish (Raphanus sativus L.) leaves. (From Sanchez, C.A., Phosphorus, in Handbook of Plant Nutrition, A.V. Barker and D.J. Pilbeam, (eds.), CRC Press, Boca Raton, FL, 2007, pp. 51–90.)

As P is mobile in plants, sampling and analysis of new growth usually are recommended to ascertain the current status of P uptake. Phosphorus is incorporated into the structure of many cellular compounds, so it is possible to have a relatively high P concentration in the overall tissue, while also having a deficient level of soluble phosphate that is needed for the chemical transactions that require it. Therefore, in many instances, researchers have found that the best tissue to sample is that which contains the pipeline of vascular tissue. Cotton, sugar beet, and potato are examples of plants that commonly are managed for in-season nutrient status by sampling and analyzing petiole tissue connecting leaves to stems.

Westermann and Kleinkopf (1985) found that potato yield is related to the number of days from the time of tuber initiation where the shoots contained greater than 2.2 g P kg−1 dry mass, which correlated to 1 g soluble P kg−1 in the fourth petiole from the top of the plant. Walworth and Muniz (1993) published a compendium of potato nutrient concentrations in which they defined the “ sufficient” level for various plant parts at different stages of growth, with midseason leaf-blade sufficiency at ≥2.6–4.7 g P kg−1 and midseason petiole P sufficiency of ≥1.5–3.1 g P kg−1. Recent work by Freeman et al. (1998) suggested critical petiole total P levels for “Russet Burbank” of 4.5–5.7 g P kg−1 when tuber length is 5–10 mm, 3.5–4.7 g P kg−1 at 35–45 mm, and 2.1–2.6 g P kg−1 at 75–85 mm, although work by Sanderson et al. (2003) and Rosen and Bierman (2008) was less definitive. Work in Idaho showed a sufficiency level of >2.2 g P kg−1 (Stark et al., 2003).

Potato tissue analysis has been studied more and is used more commonly as a management tool in commercial production than for most of the top global crop species, with most growers sampling the crop on a weekly basis during the time of tuber initiation until canopy senescence. However, other species are also managed actively with tissue analysis. Figure 3.8 shows yield response curves for lettuce sampled at various timings through the growing season. It is noteworthy that, in the case of lettuce, soluble acetic acid–extractable phosphate is analyzed rather than total P. Other species are managed using this extraction rather than total P concentration.

Critical acetic acid–extractable phosphorus at four growth stages of lettuce (

Figure 3.8   Critical acetic acid–extractable phosphorus at four growth stages of lettuce (L. sativa L.). (From Sanchez, C.A., Phosphorus, in Handbook of Plant Nutrition, Barker, A.V. and Pilbeam, D.J. (eds.), CRC Press, Boca Raton, FL, 2007, pp. 51–90.)

Similar information is available for a wide variety of other species for P, such as for corn, soybean, pecan (Carya illinoinensis K. Koch), tomato, and lettuce (Sanchez, 2007). Sanchez (2007) and Mills and Jones (1996) provide a listing of plant tissue concentrations for hundreds of species identified by sufficiency ranges as determined by research or, if insufficient information is available, by survey range or average based on nutrient concentrations found through routine analysis in their laboratories. The key is to sample each species uniquely by following established sampling protocols and taking tissue from parts that are highly correlated to P status and relate to fertilizer decisions.

3.8  Forms, Concentrations, and Bioavailability of Phosphorus in Soils

3.8.1  Three Pools of Soil Phosphorus

Phosphorus exists in solid form as part of the structure of a wide variety of soil minerals, such as rock phosphate, present as fluorapatite [Ca5(PO4)3F] or hydroxyapatite [Ca5(PO4)3OH]. It is also present as precipitated forms on other soil and rock particles. Inorganic mineral forms in soil are not found in any typical ratios, but tend to be combinations of sorbed/precipitated P on amorphous Fe and Al oxides and hydrous oxides and CaCO3 2− (Cole et al., 1953; Griffin and Jurinak, 1973; Holford and Mattingly, 1975).

The organic fraction is also an important pool of solid P in soils, existing predominately as the easily degraded phospholipids (~1%) and nucleic acids (5%–10%) and their degradation products, along with the more stable inositol polyphosphates (up to 60%), which are part of the humus fraction of soils (Anderson, 1967; Halstead and McKercher, 1975; Ko and Hora, 1970; Omotoso and Wild, 1970; Steward and Tate, 1971). There are many other organic P compounds, consisting of components of living organisms and their degradation products, with many of them unidentified complex compounds. Soil microbes degrade other organisms and release organic P, including by enzymatic cleavage via phosphatases (Alexander, 1977; Anderson, 1975; Cosgrove, 1977; Feder, 1973).

Plants absorb nutrients from the solution phase and not directly from the solid phase (Figure 3.9). Therefore, solid forms must be converted to liquid and chemically converted to mono- or diprotonated phosphate (HPO4 2− or H2PO4 ) before plants can obtain P. Unfortunately, total P concentrations are much higher in the solid phase than in soil solution (Young et al., 1985). Bioavailable dissolved P concentration in the soil solution is typically very low; the median is 0.05 mg P kg−1 compared with the 200 to >1000 mg kg−1 total P typical in soils (Young et al., 1985). Although solution P levels are usually low, there is variability across soils as dictated primarily by soil pH and the presence of various cations, minerals, and organic compounds (Lindsay, 2001; Sposito, 2008).

Some soils have unusually high solution P levels, typically those that have been very highly amended with manure or similar organically complexed P materials (Alva, 1992; Bradley and Sieling, 1953; Davenport et al., 2005; Holford and Mattingly, 1975; Kissel et al., 1985; Lindsay 2001; Nagarajah et al., 1970; Sharpley et al., 2003; Sposito, 2008). Erich et al. (2002) found that soils amended with compost and manure developed higher plant-available and desorbable P. Fixen and Bruulsema (2014) state that some studies have shown that soluble organic compounds can inhibit P sorption in certain soils (Iyamuremye and Dick, 1996) but can increase P-sorption capacity in various tropical soils (Guppy et al., 2005). Malik et al. (2012) suggested that organic P sources can stimulate the formation of slow-release organic P forms. However, use of living cover crops to keep P in a more soluble plant-available form has mixed results (Little et al., 2004).

Much of the P taken up by plants is provided by the mineralization of organic materials, but release from minerals is also important. Minerals break down very slowly over time and can release structural P, but this amount represents very little of the P that plants take up in any one growing season. The majority of P supplied to plants comes from desorption of precipitated mineral deposits. However, this process is generally very inefficient because the phosphate molecules are poorly soluble and, as such, can quickly precipitate back out of soil solution as P cycling occurs.

Phosphorus soil cycle.

Figure 3.9   Phosphorus soil cycle.

In summary, soil P exists in three pools of availability, although the actual system is much more complex. The bioavailable P is the soil solution P (often termed the intensity portion). The labile P is the P in readily soluble form (termed the quantity factor). This labile fraction typically includes poorly sorbed mineral P, soluble P minerals, and easily mineralizable organic P. The other pool is the nonlabile P, which is strongly sorbed P, insoluble P minerals, and organic forms resistant to mineralization and cleavage of P.

3.8.2  Phosphorus Equilibrium in Soil

Precipitation/adsorption of P occurs rapidly due to equilibrium chemistry. Just as there is a limit to the amount of table salt (NaCl) that can be dissolved in water, the soil solution will allow only a finite amount of dissolved P (with a notable difference being that the equilibrium concentration for highly soluble NaCl is very high, but it is very low for the poorly soluble P compounds). The reverse reaction (solubilization of precipitates and desorption of labile P) also occurs, with P coming back into soil solution. The rate of this reaction accelerates when nonequilibrium conditions exist due to P being removed from soil solution. As plants take up P, a state of nonequilibrium is created, and dissolution of solid-phase P will occur until equilibrium conditions are satisfied once again. Although these sorption–desorption reactions occur and help maintain P available for plant use, the rate of the dissolution reactions may be too slow to fully meet the P demand for plants growing in some soils.

Soil water levels will have an impact on the equilibrium levels and plant availability of P, with optimum levels at about field capacity (Watanabe et al., 1960). Saturation above this optimum, although resulting in enhanced solubility of Fe-bound phosphates (Bacon and Davey, 1982; Holford and Patrick, 1979; Ponnamperuma, 1972), results in reduced P uptake for crops not adapted to saturated conditions due to poor root health under anaerobic conditions. Low soil water negatively impacts P uptake due to reduced volume of soil from which P can diffuse; it has a more tortuous pathway with higher concentration of other salts interfering in the path (Barber, 1980). Additionally, dry conditions often result in roots drawing water from lower portions of the soil profile where P is in lower concentrations as compared with the topsoil (Hanway and Olson, 1980). Soil temperature also impacts P solubility and availability as a function of increased chemical reaction kinetics and microbial activity (Gardner and Jones, 1973; Sutton, 1969).

The P concentration of the soil solution at equilibrium and, thus, plant P availability are highest at the slightly acidic to neutral pH range and are reduced considerably in strongly acidic or alkaline soil conditions. Solubility is further decreased in the presence of excessive lime (CaCO3) (Kissel et al., 1985; Westermann, 1992). Excessive CaCO3 in the soil increases P sorption on these surfaces and increases the precipitation of soil solution P as Ca–P minerals (Sharpley et al., 1989). Phosphorus combines with Ca and Mg, which are typically at high concentrations in alkaline soils. These Ca–Mg phosphates are poorly soluble at high pH. A similar reaction occurs in acidic soils, but with Al, Fe, and Mn, with the formation of poorly soluble phosphate minerals under low pH conditions. However, George et al. (2012) offer a somewhat different view, stating that inorganic P reactions are not as important as are changes in P stability as a function of pH in most soils with levels of organic matter that are greater than about 1%.

Because of these physical–chemical issues, plants utilize only a small portion (from near 0% to ~35%) of fertilizer P in the first year after application (Jacob and Dean, 1950; Randall et al., 1985; Syers et al., 2008), with the lower end of this range more common. Jacob and Dean (1950) found that two varieties of potato took up just 5% of the fertilizer P applied. Such is the case with a typical broadcast application of traditional P fertilizers.

The remaining P not utilized by plants and precipitated out of solution is often referred to as fixed P. Fixation is an unfortunate and confusing term. As such, it is no longer used in reference to P in soil science publications but continues to be used commonly in production agriculture. Fixation refers to very different processes for N, P, and K. Unlike the fixation of K+ and NH4 + into the lattice structure of clay minerals (which removes K and NH4 + from the bioavailable pool) and N fixation of atmospheric N2 gas by N-fixing microbes (which adds N to the bioavailable pool), P fixation is defined as the formation of solid-phase P compounds formed by precipitation or strong adsorption to soil minerals. Despite what is implied with the term fixation, these precipitates and adsorbed forms of P are not all permanently lost to plant uptake, although it may take many years before plants are able to utilize most of the P from a fertilization event (Randall et al., 1985; Syers et al., 2008). This phenomenon is related to the very poor solubility and mobility of P in soil and the fact that roots tend to explore less than 1% of soil at any one time. Since a large portion of fertilizer P is not utilized by plants in the first year after application, the remaining P is available for uptake in future years. Solubility of these P minerals declines slowly with time as the P compounds formed become increasingly less amorphous and more crystalline by geologic processes via P fixation reactions (Kissel et al., 1985; Lindsay, 2001; Sposito, 2008).

3.8.3  Fate of Fertilizer Phosphorus in Soil

Fixen and Bruulsema (2014) give an excellent explanation of the physical chemistry principles of P availability from fertilizer. They state that reactions of P applied to soils can be described very broadly as sorption, precipitation, or organic interactions (Kissel et al., 1985; McLaughlin et al., 2011; Sposito, 2008). Sorption refers to the adsorption of P to the surface of soil particles, such as Fe and Al oxides or CaCO3 2−, often replacing water or hydroxyl (OH) ions through ligand exchange. These reversible reactions occur rapidly. Sorption also includes the slow penetration of P below the surfaces of these solid particles. Australian research has shown that the P-sorption capacity of soils is an important factor in determining the amount of P fertilizer required to achieve maximum yields (Hegney et al., 2000).

Fixen and Bruulsema (2014) further stated that precipitation occurs when the addition of a P fertilizer causes the concentration (activity) of P in solution to exceed the solubility product of mineral phases (Bell and Black 1970; Lindsay et al., 1962). Below these concentrations, the sorption reactions described earlier are the dominant reactions. The classic solubility diagrams of Lindsay (1979) are still the generally accepted chemistry of the thermodynamic relationships believed to occur. When soluble fertilizers are added to soil, the most soluble minerals precipitate first because the reactions are faster. There are more ions in solution and a greater chance that collisions with nucleation sites will take place and cause the mineral to grow. With time, the P in soil solution declines due to incorporation into the more soluble minerals, and those same minerals then begin dissolving. The P contained in them precipitates as the less soluble mineral phases grow. So, as time passes, there is a cascade of P from soluble to less soluble minerals forming.

Lindsay (1979) states that Al and Fe phosphates are the most stable (least soluble) forms in acidic soils and Ca phosphates are most stable in alkaline conditions. However, Fixen and Bruulsema (2014) state that recent studies using direct spectroscopic techniques show that soil P is not always behaving as stated by Lindsay (1979), likely due to factors that influence reaction kinetics and the numerous potential reactants in soil solutions that could create somewhat messy mineral phases. For example, significant calcium phosphate minerals have been identified in moderately acidic soils, while Fe oxides have been found to be active sorbers of P in alkaline soils.

Fixen and Bruulsema (2014) summarize the sequence of events following fertilizer P (as MAP) addition to soil as follows:

  1. Upon addition to soil, capillary flow of water into the granule begins—bringing Al, Fe, and Ca along with it. This process occurs at the same time P is diffusing out of the granule. This action is much less important with fluid NH4 + phosphate forms, such as APP. The flow into the granule can impact the diffusion of P from the granule. Spectroscopic evidence exists that in some soils the flow into the granule results in precipitation of the mineral crandallite, a Ca–Al–OH phosphate (Lombi et al., 2004). Most of the P leaves the granule in a matter of days, but crandallite residues can remain for months.
  2. As P leaves the granule, much of it quickly precipitates as several different forms of NH4 + phosphate, since NH4 + is also diffusing from the granule. These new NH4 + phosphates are still very soluble, but less soluble than MAP. Changes in pH and other solution factors are the driving forces behind this precipitation.
  3. As the NH4 + diffuses away from the reaction site or nitrifies, the NH4 + phosphates dissolve and, in nearly all temperate soils, P precipitates as dicalcium phosphate dihydrate (Ca2HPO4 · 2H2O), which is a somewhat soluble P form, although much less soluble than the original fertilizer.
  4. The soil pH then largely dictates subsequent reactions: In moderately acidic soils, P minerals containing Fe, Al, or Ca precipitate are formed after about 35 days. Common examples are strengite (FePO4 · 2H2O), vivianite (Fe3(PO4)2 · 8H2O), variscite (AlPO4 · 2H2O), and apatite analogs (various calcium phosphates). After about 180 days, these minerals will have dissolved largely, and much of the P is sorbed by hydrous oxides of Fe and Al or they remain as apatite analogs. In alkaline soils, P minerals containing Ca are dominant at 35 days with octacalcium phosphate (OCP; Ca8H2(PO4)6 · 5H2O) being one of the most common forms, but with apatite analogs occurring as well. Eventually, the more soluble Ca–P minerals, such as OCP, dissolve, and P is sorbed by CaCO3 or Fe oxides. Apatite analogs often are found, persisting for extended periods. The importance of Fe oxides in these alkaline soils, verified by direct spectroscopic evidence, has been surprising considering the solubility relationships described by Lindsay (1979).

Fixen and Bruulsema (2014) stated that a critical component of this cascade of reactions is the massive decline in P solubility, which occurs while these reactions between fertilizer and soil are taking place. The solubility of the original P fertilizer is very high, but the solubility of the final products is several orders of magnitude less. Cultural practices, as well as soil and environmental conditions, greatly impact the timing of the formation of these P minerals in soil. They further stated that crop P uptake in a given growing season is the sum of the P taken up by roots intercepting fertilized zones and the P absorbed from the bulk soil, with the vast majority of the P coming from the bulk soil. For example, Australian research employing P isotopes has indicated that 70% or more of crop P uptake is derived from the bulk soil (McBeath et al., 2011). We apply fertilizer P to fill the gap between what the bulk soil can provide crop roots and the P required for the attainable crop yield.

3.9  Soil Testing

3.9.1  Benefits of Soil Testing

Although plant tissue analysis is a good tool for predicting yields and in-season fertilizer needs, it needs to be coupled with soil testing. Tissue analysis is especially helpful for highly soluble and mobile nutrients, such as N. Unfortunately, P does not fit into this category of soil mobile nutrients, making soil testing an even more important management tool. Hopkins et al. (2010a,b) found that fertilizer P applied and incorporated into the soil prior to planting resulted in better yield response than when applied via fertigation. This action is logical given the fact that P applied to the soil surface will generally only move a few mm in soil once it converts from liquid to solid phase. Thus, this P is unavailable to all but surface-feeding roots, which are relatively more subject to interferences from soil heat and water limitations.

Therefore, it is vital for managers to be able to predict P fertilizer needs prior to planting through soil testing and field records so that this fertilizer can be incorporated into soil prior to, at, or shortly after planting. Typically, there is a curvilinear relationship between soil test P and yield response (Figure 3.10). The likelihood of response diminishes as the soil test P level approaches the critical level, which is defined as the concentration above which no response to added P is reasonably expected (Kissel et al., 1985; Lindsay, 2001; Marschner, 2012; Sposito, 2008; Young et al., 1985). Responses to P fertilizer are large at very low soil test P levels, with decreasing amounts needed in order to achieve full yield potential as soil test P approaches the critical level. Figure 3.10 shows the correlation between yield responses and soil test P levels for celery at 18 sites in Florida with Histosol soils, illustrating the development of a critical level unique to the crop, soil, and environmental conditions. Figure 3.11 shows the result of compiled fertilizer studies resulting in a P fertilizer recommendation rate chart as a function of soil test for celery, lettuce, sweet corn, and snap beans.

Critical soil-test phosphorus levels (by water extraction) for production of large, harvest-size celery (

Figure 3.10   Critical soil-test phosphorus levels (by water extraction) for production of large, harvest-size celery (Apium graveolens Pers.) on Florida Histosols. (From Sanchez, C.A., Phosphorus, in Handbook of Plant Nutrition, Barker, A.V. and Pilbeam, D.J. (eds.), CRC Press, Boca Raton, FL, 2007, pp. 51–90.)

Recommendations for phosphorus fertilization for selected crops on Everglades Histosols. (From Sanchez, C.A., Phosphorus, in

Figure 3.11   Recommendations for phosphorus fertilization for selected crops on Everglades Histosols. (From Sanchez, C.A., Phosphorus, in Handbook of Plant Nutrition, Barker, A.V. and Pilbeam, D.J. (eds.), CRC Press, Boca Raton, FL, 2007, pp. 51–90.)

Soil testing is not a perfect tool, but several methods are available and are moderately correlated to yield for various soil and crop combinations. Phosphorus soil tests are estimates of bioavailability and are index values. This testing is in contrast to other tests that are quantitative. For example, the NO3–N test is designed to extract all of this form of N from soil for analytical determination and interpretation. In contrast, the amount of P extracted from a soil includes the very small quantity of solution P plus a variety of labile solid soil P forms, none of which are fully plant available. For example, a Timpanogos loam extracted at the BYU Environmental Analytical Lab had 1645 mg P kg−1 of total P (including all mineral and organic components of the soil). Of this quantity, only 0.04 mg P kg−1 was soluble and available for immediate plant uptake. Neither of these extractions are valuable for predicting the P status of a soil in terms of plant availability. As previously mentioned, the first attempts at soil testing included analysis of total P and had poor correlation to actual P availability to plants, with many soils having high total P concentration but very low bioavailable concentrations and vice versa. As also previously mentioned, the amount in soil solution at any one time is minute in comparison to what the plant takes up during the season. For this reason, other soil-testing methods were developed to extract the most readily soluble forms of P that can be correlated to plant uptake.

3.9.2  Soil Test Methods

Sanchez (2007) reviews various soil P tests and their modes of action. Although several methods have been introduced over the last century, the three most common tests for estimating P in the United States are the Bray P1, Olsen bicarbonate, and Mehlich III. All of these tests are indexes for bioavailability. The Bray P1 method was developed originally in the Midwestern United States by Bray and Kurtz (1945) and was well correlated with plant P uptake and yield response in corn and many other crops. However, as the concept of soil testing moved westward, it was discovered that this method did not work well in the calcareous soils common in arid and semiarid regions (Mehlich, 1978). The reason for this problem was that the Bray P1 method relies primarily on a weak acid to extract the P, but the soil CO3 2− effectively neutralizes the acid and alters the results, giving false low values. As such, Olsen et al. (1954) developed a neutral salt extraction method using bicarbonate (HCO3 ) designed to be utilized in calcareous soils. This method correlated well with plant P uptake and yield. Although intended for calcareous soils, it also worked well in acid and neutral pH soils. Later, the soil-testing movement sought to reduce the cost for labor and chemicals, and as such, universal extractants were developed, which were designed to extract a majority of the essential nutrients from soil with one procedure for a wide variety of soils (Hanlon et al., 1984). Mehlich (1984) developed an extractant from a buffered acid solution. This test correlated well with P nutrition in plants under most soil conditions. Many other soil-P extractants have been developed, but although many are well correlated to P nutrition, they lack widespread adoption. There are other tests available (such as P-sorption isotherms, P fractionation, and isotopic dilution), but they tend to lack calibration data with yield or are too labor intensive to be used for routine soil testing.

It is important to realize that the results of these bioavailability tests must be converted to usable P fertilizer recommendations. Also, the analytical values cannot be related directly to an amount of P that is precisely available for plant uptake. In the case of NO3–N, it is possible to convert the concentration to a quantity of N available to plants on a kg ha−1 basis by multiplying the concentration in the soil by the depth of the soil sample and converting to the proper units. This process is done legitimately because all of NO3–N is extracted quantitatively from the soil and, assuming it is not lost via leaching or by other processes, it is all plant available. However, many growers and agronomists erroneously employ the same mathematics for P and other nutrients that are extracted using a bioavailability index method. This process should not be done since the commonly used P tests are not quantitative. When a soil P extractant is added to the soil and then shaken for a set period of time, the chemicals dissolve a portion of the labile P, but not all.

For example, the Timpanogos soil cited in the preceding example also was extracted with all three of the common methods described earlier, as well as a variety of fractionation methods to determine organic P, Ca-bound P, Fe-bound P, Al-bound P, etc. All of these extractions resulted in different P concentrations extracted from the same soil as a function of the types and strengths of chemicals added, time of shaking, heat of the solution, etc. Obviously, none of these extracts represents precisely the amount that is plant available, but rather, in the case of the bioavailable extractants, an index of P availability that requires field calibration. The results of the bioavail-ability tests were 10, 19, and 21 mg P kg−1 for the Olsen bicarbonate, Bray P1, and Mehlich III extractions, respectively. The mistake that is made commonly by growers and their agronomists is to convert these concentrations to what they assume to be the equivalent of fertilizer P. In this case, the results would be 20, 38, and 42 kg P ha−1 or, in terms of fertilizer amounts, would be 45, 86, and 95 kg P2O5 ha−1 for the Olsen bicarbonate, Bray P1, and Mehlich III extractions, respectively. They then look up the amount of P taken up or removed by a crop, such as what is shown in the last column in Table 3.2, and then subtract the amount from their calculation to determine the fertilizer rate to be applied. One can see, however, that each of the methods gives a very different result and may lead one to ask which method is correct. The problem is that this is not an appropriate way to determine fertilizer rate.

Rather, the values from these extracts should be interpreted based on fertilizer trials used to correlate fertilizer response to soil test level, such as is shown in Figure 3.10. What is the likelihood of a fertilizer response at 6 mg P kg−1? The answer is dependent on which test was employed. If this value was the result of a total soil P analysis, this would be an impossibly low number and meaningless due to a lack of correlation for fertilizer recommendation. If this is a water-extractable value, this value is impossibly high and, again, meaningless. If it was from the same extraction used to develop the yield response curve in Figure 3.10, then we can legitimately interpret the data to show a high probability of response. In this case, a 6 kg P ha−1 value would mean that we would probably only achieve about 65% of maximum yield without fertilizer.

It is important to understand that each soil extractant will result in its own unique response curve with varying results. For example, a value of 20 kg P ha−1 for the Olsen bicarbonate test would be high for most crops and no fertilizer would be recommended, but the Bray P1 and Mehlich III tests tend to be about twice as high, and therefore, a value of 20 kg P ha−1 may trigger a recommendation to apply fertilizer P based on field calibration showing responsiveness at this level. The main point here is that data from each extractant have to be interpreted based on its own independently developed data set calibrating it to crop response to P fertilization.

Some researchers have attempted to make direct comparisons between the commonly used tests (Bishop et al., 1967; Fixen and Groove, 1990; Hooker et al., 1980; Kamprath and Watson, 1980; Kuo et al., 1996; Maier et al., 1989b; Mallarino, 1997; Smith and Sheard, 1957; Thomas and Peaslee, 1973). Maier et al. (1989b) compared eight extractants at 33 locations and determined that the potato critical values were 17 and 26 mg kg−1 for the Bray P1 and Olsen bicarbonate extractants, respectively. The other extractants evaluated did not correlate well under the conditions of their study. This is just one example, but other comparisons exist. It is advisable to use a soil test method for which there are calibrated data for valid comparisons.

Ideally, a soil extractant has been vetted fully with fertilizer response research trials for each crop and soil combination possible, with the results showing at least an adequate relationship between extractable P and crop yield parameters of interest with a significant response to P fertilization when the extracted amount of P is low. There are plenty of examples of such research results, but the reality is that there are large gaps in the data due to time and budget constraints of the scientific and agricultural communities. Not every crop has been tested under every soil and environmental condition, and untested cultivars may have unique requirements. The response curve is likely to change even within a species with differences between cultivars or with differences across soils and environments. For example, in potato, there is a wide range of critical levels varying by time (Johnston et al., 1986), soil type and texture (Birch et al., 1967; Bishop et al., 1967; Boyd and Dermott, 1967; Giroux et al., 1984; Kalkafi et al., 1978; Kelling and Speth, 1997; Maier et al., 1989b; Redulla et al., 2002), and cultivar (Freeman et al., 1998; Maier et al., 1989a; Murphy et al., 1967; Sanderson et al., 2003). In the work of Johnston et al. (1986), these researchers determined the critical level for potato with the Olsen bicarbonate test was at 25 mg kg−1, but this value varied between 10 and 54 mg kg−1 between years. Similar findings have been discovered for other crops as well. These varying results might leave one doubting the value of soil testing.

3.9.3  Customization of Soil Testing

However, soil testing is a proven method, even if not perfect, and it is certainly better than not having any assessment of soil P status. Additional research is needed to fine-tune P fertilizer recommendations based on soil testing. For example, it was discovered that adjusting the P fertilizer recommendations based on the concentration of free lime in the soil significantly improved accurate prediction of P response (Lang et al., 1999; Stark et al., 2004; Westermann, 1992). Other researchers have begun to use Al analysis to adjust P recommendations (Khiari et al., 2000). Additional research is needed to examine these and other adjustments that may improve soil test correlations with yield response.

Furthermore, soil test data should be combined with field records of yield performance along with records of tissue analysis and long-term soil P trends to fine-tune future fertilizer recommendations in order to customize fertilizer recommendations for individual fields. For example, an alfalfa field in Idaho had a medium–high soil test of 15 kg P ha−1 (Olsen bicarbonate). However, analysis of the harvested hay from this field revealed that the P content was unusually low, especially in the cuttings later in the season. Field records showed that other crops grown in this field previously also trended low during the later part of the season. The farmer and his agronomist conducted a fertilizer strip trial in this field, showing significant yield increases with modest amounts of P fertilizer despite the soil test interpretation indicating that none was needed. The soil testing did not fail, but rather this particular soil was below average in terms of its ability to desorb P to provide for late-season plant needs. The soil test interpretations were then adjusted for this soil type in making future P recommendations.

Another important factor to consider when soil testing is the spatial variability of soils and other conditions. Most fields contain a variety of conditions and soil types. It is not uncommon to have areas of a field that are deficient in P when the field average is showing adequate or even excessive P availability. This occurrence is especially true in fields with eroded hilltops with exposed subsoil having very low bioavailable P levels. Subsoil is typically low in organic matter and plant-available P and high in pH and antagonistic (for P and many micronutrients) calcium carbonate (CaCO3), magnesium carbonate (MgCO3), gypsum (CaSO4), or sodium bicarbonate (NaHCO3). Calcium in particular is a known antagonist for P availability to plants. Spatial differences also can develop in the opposite situation in areas of fields that are especially productive and result in greater nutrient removal rates as a function of continual above-average yields.

If only one representative sample is taken per field, it is likely that portions of the field will have suppressed yields in cases where fertility levels are below the average. Over the years, this situation has resulted in growers having their faith in soil testing shaken when, in fact, the problem lies with poor sampling and interpretation. Various methods to account for spatial variability within fields can be employed, but at a minimum, samples should be taken from unique areas likely to be less fertile than the field average. Technology exists to variably apply fertilizer to the areas that are in need with none applied where the P levels are high.

Another approach to soil testing is the use of ion exchange resins (Jones et al., 2013). The concept here is that a porous bag containing the resin lies in the soil and undergoes conditions similar to those plant roots will experience. The soil solution then interacts with the resin, with nutrient absorption taking place. Later, the resin capsule is removed from soil and the nutrients are extracted and analyzed. Although the claim that this system is more true to the mechanisms of nutrient uptake (as compared with extracting a soil by adding chemicals, shaking, and filtering) is partially true, the resins can be located only in one place in the soil, whereas roots expand into the fertile topsoil along with deeper horizons. And, although diffusion toward the resin can occur, mass flow and root interception mechanisms are not operating. Furthermore, there is a lack of rhizosphere interaction with proton and organic acid and other root exudates. Research results are mixed with regard to whether the resins are better or less satisfactory predictors of P availability compared with conventional soil tests.

3.10  Phosphorus Fertilizer Management

3.10.1  Phosphorus Fertilizer Importance and Conservation

Successful civilizations are built largely on a foundation of agricultural productivity. A populace with plentiful and inexpensive food is then free to pursue advances in education, communication, engineering, transportation, etc., because the majority of their time and efforts are not focused on providing their next meal. Such is the case for many of the impoverished nations of the world. Furthermore, many civilizations have failed due to the loss of soil or soil productivity. Such losses contributed to the demise of the Fertile Crescent, the Roman Empire, and the Incan Empire, as examples (Pointing, 2007). George Santayana (1863–1952) coined the saying that “Those who cannot remember the past are condemned to repeat it.” If humankind hopes for continued prosperity in developed nations, the good earth that currently provides food, fuel, and fiber for more than seven billion people must not be ignored. Achieving prosperity in developing nations hinges upon a high level of self-sufficiency with regard to crop production. Crops contain nutrients, and their removal through harvest and transport to population centers depletes soil fertility. The law of conservation of mass applies insofar as matter, including plant nutrients, can be neither created nor destroyed. In other words, when minerals are removed from the soil, they must eventually be replenished through the colossally slow process of rock minerals breaking down naturally or through the addition of fertilizers.

The manufacture of fertilizer, however, is not without cost of resources, some of which may be eventually exhausted. The majority of P fertilizer used is in mineral form. The resources used include mined P and S minerals (elemental S used to create H2SO4, which is then used to create H3PO4 from rock phosphate) and fossil fuels for heating during the manufacturing process, as well as natural gas used in the manufacture of N fertilizers. Some of these resources are finite, and all are worthy of conservation. There is much speculation and study on when these resources might be depleted, with some arguing that we will run out of rock phosphate resources and fossil fuels within decades (Cordell et al., 2009; Marschner, 2012). However, these estimates are far too extreme (Van Kauwenbergh et al., 2013). Current sources, along with known undeveloped resources and improvement in mining and recovery technology, mean that the Earth’s vast resources will provide phosphate rock for fertilization for many centuries. Regardless, we owe our best efforts of conservation to future generations. We do not want to duplicate the actions of the infamous Easter Island inhabitants who, beginning many centuries prior to their failure, squandered their natural resources to the point of collapse.

There are at least two avenues of conservation. Philosophically, society should be recycling back into soils human and other animal wastes, as well as other wastes from products generated via fertilization of crops. Loss to water bodies should be avoided as much as possible, as P recovery from lake and ocean sediments is not realistic with current technologies. Ideally, these wastes should be applied to the land from which they came, but this act is not practical under current policies and conditions. Typically, crops are transported to centers of animal production and human populations and the wastes are largely applied to land in that locale. This movement results in depletion in the areas of crop production and accumulation near the animal production centers. Transporting animal manures back to the point of origin of the crops from which they came comes at a cost that society is currently not willing to pay. Even if society was willing to transport these wastes, there is an argument again because of the use of fossil fuels that would be required, as well as the pollution derived from the exhaust. Alternatively, many propose that crops should be locally produced, with waste products recycled back into soils, but this would result in increases in food production costs under current conditions.

Even if the ideal of directly applying nutrients from waste back to the soil from which they came was possible, there would not be enough to meet the demand because the system is leaky and solubility of P decreases over time. Recycling P is thwarted partially due to soil reactions described previously, with the cascade of increasing less soluble P minerals forming over time. In other words, recovery of fertilizer P is never 100% efficient. The other inefficiency is due to the leaky nature of the P cycle. Some of the P in the waste stream inevitably enters the surface water system and eventually ends up as sediment in streams, lakes, and oceans. This process occurs through point source (such as from sewage treatment facilities) and nonpoint source (such as soil erosion and P transport via precipitation runoff) avenues of loss. It is not reasonable to stop the loss of P to water completely, but this action should be the goal as much as it is reasonably possible to do so.

Therefore, mineral fertilizers continue to be an important resource to replenish nutrients lost through crop harvest and will remain so indefinitely. In an effort to lead in the wise use of resources, the fertilizer industry has adopted the 4 Rs of fertilizer stewardship, which are choosing the (1) right rate, applying the correct rate based on experimentation under various environmental conditions; (2) right timing, ensuring peak nutrient availability at the time of greatest uptake; (3) right placement, concentrating nutrients in the soil at locations where there is a large volume of roots; and (4) right product, using sources that are soluble and have release patterns conducive for plant uptake. In addition, factors that enhance root–soil contact will increase PUE (Hopkins et al., 2014).

3.10.2  Phosphorus Sources

Before discussing specific P sources and considerations, it is important to understand fertilizer labeling. The laws in many countries require that any product sold as a fertilizer must contain a guaranteed analysis of the primary macronutrients in the order of N–P2O5–K2O. Due to misconceptions regarding the chemical compositions of fertilizer materials at the time of the creation of the fertilizer laws, P is expressed on a container of fertilizer as P2O5 rather than its elemental composition, or as it is typically found (as phosphate) in most P fertilizer. For example, the sellers of 0-45-0 are claiming a minimum of 45% P2O5, which is 45 kg P2O5 for a 100 kg unit. The oxidized state of P is actually PO4 3− and not P2O5, but the laws and tradition have institutionalized this labeling. It is not likely to change in the future. This labeling is unfortunate because, although P is expressed consistently as P2O5 for fertilizer, there is a lack of consistency in how P is expressed for concentrations and quantities in plants, soils, and waste materials, sometimes being expressed in the oxide form (either P2O5 or PO4) and sometimes in the elemental form (P). This variability frequently causes confusion, and therefore it is important to understand which form is being expressed when dealing with P nutrition data. Converting from elemental P to fertilizer rate is accomplished by multiplying P2O5 by 43.7%. For the 45 kg of P2O5 in the preceding example, there would be 20 kg of elemental P in this fertilizer.

There are several considerations when choosing a fertilizer source. The first is effectiveness of the material. In the case of P, the material needs to be water soluble or at least should have an eventual slow or controlled-release rate that is predictable. Unless a slow or controlled-release pattern is desirable, P fertilizer should be at least 60% water soluble and slow or controlled-release materials need to be similarly water soluble within the course of a growing season. Most traditional sources, such as MAP and DAP, are greater than 90% soluble. If compared fertilizers have a similar solubility, the choice of which source to use becomes one of price, availability, convenience of application, and accompanying nutrients.

Phosphorus fertilizer materials generally are blended with other nutrients. A PO4 3− anion has to be combined with cations (such as NH4 +, H+, K+, Ca2+, Mg2+) to maintain electrical neutrality. The vast majority of P fertilizers used globally are ammoniated phosphates, such MAP, DAP, and APP. Orthophosphate (phosphate ion) is found in MAP and DAP. APP contains polymerized phosphate ions created through dehydration prior to ammoniating. Generally, N also is needed by plants, and the blend is effective in supplying P and a portion of the N need of crops. Historically, TSP was popular, but the recognition of the synergy between NH4 +–N and P, perceived problems with P availability in certain soils, and fertilizer industry nuances have resulted in a decline in its use. There are other mineral fertilizers available as well, such as monopotassium phosphate (MKP; KH2PO4; 0-52-34), but these are utilized in small quantities.

There are also a wide variety of organically complexed P products, such as raw manure, treated biosolid waste, composted manures, and other wastes, recycled crop residues, blood meal, and fish meal. Immediate water solubility of these materials is not relevant as the release of P is typically dependent upon the mineralization of the organic materials, a process that eventually breaks down the complexed P molecules into plant-available phosphate. Plant availability of P from manure is estimated at between approximately half to nearly the same as compared with mineral P fertilizers, with release occurring mostly in the first year after application but extending into subsequent years as well (Abbott and Tucker, 1973; Curless et al., 2005; Elias-Azar et al., 1980; Gale et al., 2000; Gracey, 1984; Laboski and Lamb, 2003; Meek et al., 1979; Motavalli et al., 1989; Powell et al., 2001).

Much of the P in manure is present as orthophosphate and, as such, is immediately plant available. But a large portion is organically complexed and released slowly. This slow release can be an advantage, as long as the P is supplied in a timely fashion that coincides with plant need, which is sometimes difficult to predict and control. As previously mentioned, availability of P early in the season is critical, and yet, these materials depend upon temperature-driven microbial decay, possibly resulting in delayed release and early-season P deficiency unless adequate amounts of immediately water-soluble P are present as well. Although manure or biosolid material can serve as a very good source of nutrients, there are many potential downsides, including presence of weed seeds, nutrient imbalances, odor, presence of toxins, cost of transportation, and compaction of soil due to heavy axle loads from application. Nevertheless, proper utilization of these by-products is an effective way to recycle P and other nutrients.

Manufactured slow- and controlled-release fertilizers are engineered to release P over time (Hanafi et al., 2002; McLean and Logan, 1970; Yanai et al., 1997). In some cases, release of P from these products also is temperature controlled, having the same problem as organically complexed P early in the growing season. However, others have a time-release mechanism that is not temperature dependent. Unlike soluble nutrients, such as N, problems with fertilizer P efficiency depend more on complexation in the soil than on leaching or gaseous loss from the system (Hanafi et al., 2002; Kissel et al., 1985; McLean and Logan, 1970). Adding immediately soluble P fertilizer results in a temporary increase in soil solution P concentration at levels that exceed chemical equilibrium constants, forcing precipitation of phosphate minerals. A slow or controlled-release P fertilizer may minimize the formation of these phosphate compounds as the soil solution P concentration does not spike at as high a level and the P is released gradually over time as a function of temperature and moisture, with increased PUE as the potential result.

Organically certified P fertilizer is another avenue of fertilization that is popular with many home gardeners and required for organically certified produce (Hopkins and Hirnyck, 2007). The term organic here should not be confused with organically complexed P referred to previously. The latter is an organic compound, which is defined as a molecule containing C covalently bonded to other atoms (not including salt-forming ionic compounds containing C, such as urea fertilizer [CO(NH2)2], CO2, and CO3 2−). In contrast, Hopkins and Hirnyck (2007a) describe organic production as an ecological production management system and as a labeling term to denote products approved under the authority of the Organic Foods Production Act (in the United States). Traditional P fertilizers and many organically complexed fertilizers, such as raw manure, are not automatically certified organically. Composted manure and other products can become certified if their manufacturer meets the conditions of certification. These products can be effective P sources.

One example of an inefficient organically certified P fertilizer is untreated rock phosphate. This material is very insoluble and, as such, is a poor source of plant-available P in anything but highly acidic soil. Although this and similar materials, such as some untreated bone meals, are advocated commonly for use, applying it as a source of fertilizer is a poor choice from the practical view of P solubility and also from a philosophical view since this represents a wasteful use of the finite rock phosphate reserves.

Another point to be made regarding organically certified fertilizers is that any P atoms finding their way into a plant are chemically indistinguishable from P from any other source. It is not safer, does not make food taste any better, and is the same in every respect. There are other differences possible between organically certified and traditional fertilizers. For example, the reason that DAP, MAP, and APP are not eligible for organic certification has to do with the use of fossil fuels in the manufacture of the NH4 +, but there is no evidence that these sources of P result in unhealthy conditions for plants or for animals consuming them. There are other important considerations when comparing these sources, such as the possible presence of weed seeds, nematodes, insects, and pathogens found in manures and biosolids unless they are treated to kill these organisms. Modern consumers are, as a whole, misinformed by much of the terminology surrounding organic and related terms, such as natural as used in foodstuffs.

Engelstad and Teramn (1980) reviewed the effectiveness of P fertilizers. There are differences across sources, but most data show that equal rates of soluble P result in approximately the same plant response regardless of sources used. Again, an atom of P is the same regardless of whether it came from bones, rock, or manure, as long as it enters the soil solution and then the root. However, there are other differences that may be important as affecting uptake probability.

One difference between fertilizers is the reaction pH values (MAP = 3.5, UAP and DAP = 8.0, TSP = 1.5, and APP = 6.2; Young et al., 1985). However, the pH in the microsite around the fertilizer does not remain acidic for long, and the uptake of P is not impacted much because of the difference in reaction pH among sources (Young et al., 1985). Other fertilizers in the band, particularly N, can also have an effect on pH, most commonly an acidifying effect when nitrification occurs. Rhue et al. (1981) found that APP resulted in reduced P uptake and potato tuber yield and quality compared with DAP on soils with pH of about five. The effect was likely due to the further reduction in pH in the banded application with the APP, which has an acidic reaction pH, as opposed to DAP with an alkaline reaction pH. Young et al. (1985) stated that, in general, there are no major differences across traditional fertilizer P sources in terms of impact on crops, although some studies show minor differences. They speculated that these differences likely were due to pH or micronutrient interactions.

Another difference that can be important is that DAP can result in greater volatilization of NH3 or accumulation of nitrite (NO2 ) than MAP due to this short-lived reaction pH and, thus, may be more damaging to seeds and seedlings when in direct contact (Armstrong, 1999). High applications (≥270 kg P2O5 ha−1) of DAP or UAP placed near (≤5 cm) or in contact with potato seed piece delayed emergence, reduced stand, and negatively affected yields (Chu et al., 1984; Fixen et al., 1979–1981; Meisinger et al., 1978). When growing vegetables on very alkaline soil and with high rates of P, DAP is avoided to prevent toxicity to these small-seeded species. The popularity of MAP and DAP is due to a high analysis of water-soluble P, which results in low per unit transportation costs. In contrast, a composted manure with 1% P has transportation costs more than 50 times greater per unit of P than MAP. This cost becomes commercially unmanageable if transporting more than a few miles.

Liquid fertilizers also tend to have higher transportation costs due to lower analysis from extra water weight. The most popular liquid fertilizer is APP because its P analysis is relatively high compared with most other liquids, although lower than MAP and DAP. It is a common myth that the polymerized phosphate molecules in APP are less plant available as the phosphate chains quickly turn to orthophosphate once hydrolyzed in the soil and are available immediately for plant uptake. Legitimate reasons cited for using liquids over solid P fertilizers in some circumstances are homogeneity of blends resulting in uniform application, sequestering of micronutrients to aid in their uptake, ease for combination applications with liquid pesticides, ease of fertigation, no caking of solids, and advantages for the fertilizer dealer in terms of safety and equipment logistics. But if the same amount of P is applied at the same distance from a plant root, it will not likely distinguish between a phosphate ion from MAP, DAP, or APP as the P is chemically identical once entering the soil. This is true for all water-soluble forms of P.

Comparing liquid with various forms of solid P fertilizer in potato, sources have been shown to result in differing yield results. Stark and Ojala (1989) reported yields 9%–15% higher with band-applied APP than with acid–urea phosphate in potato grown in a calcareous Idaho soil. Locasio and Rhue (1990) reported yields 20%–40% higher with APP or TSP than with DAP on a slightly acidic sand soil in Florida. However, DAP resulted in higher yields compared with APP (Rhue et al., 1981), as well as being better than MAP (Sanderson et al., 2003) and TSP (Giroux et al., 1984). However, MAP or TSP had higher yields than APP in Michigan (Christenson and Doll, 1968). Given these convoluted results and other researchers reporting no source differences, it is recommended to choose a source based on pricing and convenience factors (MacLean, 1983; Rosen and Bierman, 2008).

Another source issue is the common practice of the mixing of several nutrients to make up a fertilizer product. Phosphorus fertilizer is mixed commonly with K and/or the secondary macro-nutrients and micronutrients to make a more complete mixture. These mixtures can be problematic due to segregation of fertilizer prills of differing size, density, and shape and can result in uneven applications. This problem is especially true when using broadcast spreaders throwing the material a long distance. Again, using a well-mixed liquid blend eliminates this problem. Also, this problem can be eliminated for solid fertilizers by liquefying and mixing the nutrients and then solidifying into an even blended material.

A potential drawback of these blends is that a nutrient that is not needed based on soil-testing results may be applied wastefully. This waste is especially common in the urban fertilizer market. Most fertilizer materials available in retail outlets are solid mixtures or blends, such as a 20-10-15 (20% N, 10% P2O5, and 15% K2O). However, many urban landscapes have been overfertilized grossly, and especially, turfgrasses common to urban landscapes are particularly efficient at P uptake. Greater than 90% of soil samples processed at the BYU Environmental Analytical Lab for homeowners show that no additional P is needed, and yet most homeowners and urban landscape managers wastefully apply P due to the convenience of purchasing a fertilizer mixture. Turfgrass is the number one irrigated crop in the United States, and therefore, the amount of wasted P application is substantial. As a result of this and environmental issues surrounding P fertilizer use, many communities have instituted fertilizer bans (Hopkins et al., 2013). This approach is shortsighted. Instead, urban landscapes need to be fertilized similarly to how farmers do business by basing fertilizer recommendations on soil testing and applying custom blends rather than a “one-size-fits-all” approach. More often than not, soil and tissue analyses reveal that all of the fertilizer needs for a typical urban landscape can be met with a combination of urea and ammonium sulfate fertilizer, with no P needed in the foreseeable future.

Fertilizer prill size is another important source consideration, especially for turfgrasses and carrot and other plants that have a very narrow diameter of soil exploration by roots for each plant. For most agronomic crops, this is not an issue because of the wide circle of soil exploration by each plant. But plants with small root systems require small prill sizes for more uniform coverage of nutrient over the landscape. A large prill applied to turfgrass may result in a few plants right around the prill receiving a large dose, but those a few cm away accessing little if any of the nutrient. This result is particularly true for the poorly mobile P fertilizers, and as such, the turfgrass and specialty crop fertilizer industries have products with very small prill size that are available, although the cost is relatively high.

Other aspects related to fertilizer sources are additives and enhanced efficiency fertilizers. One very widely sold, but controversial, product is AVAIL® (Specialty Fertilizer Products, Leawood, Kansas). Hopkins (2013) reviews the proposed mode of action for AVAIL, a high charge density polymer that sequesters interfering cations. He also reviews the work performed on AVAIL and its impact on P soil chemistry. Chien et al. (2014) rebut the effectiveness of AVAIL. However, positive responses were observed and published for rice (Dunn and Stevens, 2008) and two potato studies showed mixed responses (Stark and Hopkins, 2014). Hopkins (2013) reviews other informally reported studies on a variety of crops. In some cases, yield increases have been reported, whereas in other instances, yields were not impacted or results were mixed. One conclusion from this review was that many of the nonresponsive reports cited by Chien et al. (2014) occurred on soils with medium to high soil test P where the probability of P response would be unlikely. For example, McGrath and Binford (2012) found no response to AVAIL in corn, but all of their sites had moderately high to very high soil test P and responded to starter P at only 2 of 8 sites. Karamanos and Puurveen (2011) also observed no response at two field sites with wheat grown in slightly acidic soil, one site with low and the other with high soil test P. Although Chien et al. (2014) conducted a meta-analysis on many of these studies, the fact that most were done on high P testing soils makes the analysis suspect. A similar analysis for MAP trials on high P testing soils would lead to a conclusion that MAP is not needed, when in fact it is an effective product when used on soils in need. Hopkins (2013) states that AVAIL was effective only when the rate of P was reduced. In other words, if a plant already has adequate P due to high rates of P fertilizer or residual P in the soil, AVAIL or any other P fertilizer enhancements will not likely provide any benefit.

Another approach to enhancing P efficiency is to increase solubility. Phosphorus bound to the organic acids in products such as manure, compost, biosolids, or other waste materials has been shown to increase P solubility and plant uptake dramatically when high rates are used (Bradley and Sieling, 1953; Holford and Mattingly, 1975; Nagarajah et al., 1970). This effect can last for decades and is observed commonly in soils that have a history of heavy manure or biosolid applications (Sharpley et al., 2003). There have been many efforts to harness the increase in P solubility when applied in combination with organic acids, but without having to apply the massive quantities of manures or other biosolids. This effect is accomplished potentially by adding concentrated humic, fulvic, or other organic acid additives directly with P fertilizers. Andrade et al. (2007) stated that this practice may improve PUE through a prolonged increase in P solubility. Doing so theoretically promotes the bioavailability of P without the drawbacks listed earlier. However, the sale of humic substances, unlike fertilizer sales, largely is unregulated, and products may not be reliable. Thus, buyers should work with products that are from reliable companies who can provide independent research confirmation. Plants might not benefit from additional application of organic substances in soils that are naturally high in humic substances.

Plants deficient in P have been shown to upregulate root exudation of organic acids into the soil (Grierson, 1992; Zhang et al., 1997), and it is well documented that various organic acids help to mobilize poorly soluble mineral nutrients with citrate, malate, and oxalate, the most common and effective at mobilizing P (Hoffland, 1992; Oburger et al., 2009). Their ability to reduce P precipitation (Grossl and Inskeep, 1991) and even to improve solubility of poorly soluble phosphates (Singh and Amberger, 1998) is potentially valuable in meeting plant P demands. Tan (2003) and Hill et al. (2014a,b) reviewed the potential impact of organic acids on P nutrition.

In the case of potato grown in calcareous soil, Hopkins and Stark (2003) reported that humic acid use increased plant P uptake, resulting in increased tuber quality and yield. More recent developments with use of organic acids combined with P fertilizer have been reported with a unique P fertilizer, Carbond® P (Land View Inc., Rupert, Idaho) (Hill et al., 2014a,b; Summerhays et al., 2014) for (Hopkins unpublished data). The P in this product is bonded chemically with organic acids, which is in contrast to the simple mixing of P fertilizer with an organic acid product prior to application as was reported earlier for the work of Hopkins and Stark (2003), and as is a relatively common practice in the western United States. This work is focused on low-OM soils, but recent research (Hopkins unpublished data) found similar results for moderate-OM soil, but an apparent diminished effect when soil OM was high and also found that the effect of Carbond P is not likely due to plant physiological impacts, but suggested that it is more likely related to impacts of the organic acids on soil P chemistry.

3.10.3  Phosphorus Rate

Choosing the correct rate of fertilizer P to apply has already been eluded to in the soil-testing section. Getting the right rate is a difficult proposition though. Thousands of rate studies conducted on many crops grown in a variety of soils show that the optimum rate is only somewhat predictable. There are many parameters that are integrated by the plant–soil system.

Residual soil P is an important factor impacting rate, as has been discussed previously. However, another factor is yield potential. Some soil and environmental conditions drastically limit yields. Assuming that this yield limitation is not related to P uptake, such as poor soil fertility or root or vascular system diseases, it is likely that the optimum P rate is relatively low. Evaluation of the soil system and the history of the field, including yield history, can be used to help predict rate adjustments. For example, Stark et al. (2004) provided a base P recommendation with an adjustment upward in rate of fertilizer for each increment in yield potential. A similar approach is taken in other circumstances.

Environmental conditions and many pest-related impacts on yield cannot be predicted easily. In the case of N, in-season adjustments can be made easily to cut back or add to the forecasted amount needed for the whole season. This adjustment is not as efficiently done for P due to the lack of mobility previously discussed. However, Hopkins et al. (2010a,b) found that for potato, an in-season adjustment can be made by applying P through the irrigation system if petiole tissue sampling indicates a need. Of course, a similar approach could be done by applying dry fertilizer via airplane or field spreader for nonirrigated fields, but the cost and efficiency of uptake are problematic. Furthermore, preplant-applied fertilizer obviously cannot be removed in situations where the yields are being limited due to some unforeseen problem. Although potato is somewhat efficient for in-season fertilizer use due to a prolific amount of surface-feeding roots once the canopy closes (Westermann, 2005), other crops are not as efficient. Alfalfa seems to be responsive to P fertilization on an established crop, but corn is not as efficient in its in-season uptake. Every effort should be employed to apply the correct rate of fertilizer P to plants preplant and incorporated into the soil based on soil test. Additional in-season applications should be applied if tissue analysis indicates a need and if the crop has been shown to be responsive. However, it is common that the costs for these in-season applications are higher than soil-incorporated applications and the uptake efficiency is less.

Although soil testing is a valuable tool, it is not a perfect predictor of P fertilizer need. This case is particularly problematic with potato and other inefficient P responders (Bishop et al., 1967; Freeman et al., 1998; Johnston et al., 1986). Some researchers have found soil testing to be correlated highly to plant response (Bishop et al., 1967; Giroux et al., 1984; Stark et al., 2004; Westermann, 2005), but in other studies, the results were less conclusive for tuber yield and quality responses at high soil test levels (Bishop et al., 1967; Kelling et al., 1992; Liegel et al., 1981; Nelson and Hawkins, 1947; Sanderson et al., 2003). Regardless, potato responds to fertilizer P at soil test levels higher than what is sufficient for most agronomic crops (Bundy et al., 2005). Rosen et al. (2014) stated that, due to these results and the high value of the potato crop, a method recommended by many states and provinces is to apply 50 to 100% of the predicted P removal rate (Table 3.2); even then, soil test P levels are high. This approach reduces the risk of yield loss without significantly depleting the bank of soil P and also not building it to even higher levels. However, in some cases, environmental regulations or guidelines prohibit this approach. It should be noted that fertilizing based on removal rate alone is not advisable because the rate needed is generally greater than removal rate when soil test levels are low. This approach can be used for other crops that are known to be more efficient in P response, although responses are less likely and the economics of this approach may not be justified for crops with lower value than potato.

Rosen et al. (2014) provided an excellent review of the confounding information available for P rates and stated that economical P rates for potato are clearly well above those required for most other crops. Long-term studies with corn and soybean in Iowa and Minnesota showed that applying P at crop removal rates when soil test P were in the medium range (16–20 mg kg−1 Bray P1) achieved maximum economic yields (Mallarino et al., 1991; Randall et al., 1997; Webb et al., 1992). These rates are one-sixth to one-half those required by potato and other P-inefficient crops. Most other agronomic crops are similar to corn and soybean, with typical rates near removal amounts when soil test levels are moderate.

3.10.4  Phosphorus Fertilizer Timing and Placement

Several timing and placement choices exist, including preplant broadcast either left on the surface (no or minimum tillage system) or incorporated into soil, concentrated bands applied with or near the seed, concentrated bands either applied during the season to the surface or injected between rows, in-season broadcast or applied with irrigation water, and small liquid volume foliar sprays. Each of these has pros and cons discussed below in this section.

With N fertilization, it is a good management practice to apply P in-season through slow- or controlled-release sources, with irrigation water, or as foliar or dry broadcast soil applications (Hopkins et al., 2008, 2014; Stark et al., 2004). Loss mechanisms for N result in leaching of NO3 and gaseous losses of NH3 and nitrous oxide (N2O) via volatilization and denitrification. However, the chemistry of P is very different from N, having none of these loss mechanisms. This principle is not well understood and, as such, it is common lore for growers to assume that the same constraints that hold for N will not hold for P.

Also, there is a common thought process that the cascading loss of P solubility over time is a reason to encourage in-season applications of P or recommend application directly to leaves to avoid soil interactions. Although these seem logical, they are flawed in practice due to the lack of mobility of P through soil and the inefficiency of foliar applications. Although the loss of P solubility with time is a real effect, the reality is that there is not much of a difference when comparing availability from a preplant with an in-season application a few weeks later (Lindsay, 2001; Sposito, 2008). Even when comparing a fall versus spring application, the difference in P availability is not tremendous. For instance, Stark et al. (2014) reported no significant difference between fall- and spring-applied P fertilizers for “Russet Burbank” potato. In the case of lettuce, waiting to apply P in-season resulted in crop losses compared with applying ample P preplant and without interruptions in supply (Burns, 1987; Sanchez et al., 1990). Similar findings were made for muskmelon (Cucumis melo L.) and sugar beet (Grunes et al., 1958; Lingle and Wright, 1964). Young et al. (1985) stated that timing of P application is not a critical issue in P management, as long as adequate P is available throughout the season.

As discussed previously, an in-season application of P is inherently inefficient because, unlike N and many other nutrients, P is not mobile in the soil (Lindsay, 2001; Sposito, 2008), and therefore applied P may remain in the surface layer where it is poorly available to plant roots. Broadcast and irrigated in-season applications may result in P deposition in the top few mm of soil where root biomass may be low and soil is dry. High concentration of P in surface soil is also an environmental concern because the primary P loss mechanism from soil is erosional transport into surface water (Sharpley et al., 2003), and the nearer to the surface that P is fixed, the greater the chance of erosion. The surface deposition problem possibly could be overcome with in-season P applications applied as a band knifed into the soil, but the damage from root pruning could offset the benefit of applying P fertilizer to growing plants as compared with a preplant fertilization if the knife application enters the root zone (Fallah, 1979; Stark et al., 2003; Stark and Westermann, 2008).

Despite the fact that in-season application of P is less efficient than when P is incorporated into the soil prior to or soon after planting, this practice is not completely ineffective and is sometimes necessary (MacKay et al., 1988; Westermann, 1984; Westermann and Kleinkopf, 1985). Rosen and Bierman (2008) showed a significant increase in potato P uptake and yield for split application as compared with an untreated control when the in-season application was incorporated into the soil through the cultivation and hilling process immediately prior to emergence. A later application via this method would likely have resulted in root damage, but root development into the affected area was not significant early in the season. Kelling and Speth (1997) found that in-season application of P was generally as effective as preseason application if also incorporated into the soil and if root pruning was not significant.

However, in-season applications that do not include placement into the soil are relatively inefficient (Lucas and Vittum, 1976; Randall and Hoeft, 1988). It makes theoretical sense to apply all of the anticipated P fertilizer required prior to planting in the rooting zone since timing is not a major factor. Although some species, especially perennials such as alfalfa and grasses, are adept at P uptake through roots close to the soil surface, many other species are very poor at P uptake from surface soil when P fertilizer applications concentrate it in this zone. In the case of potato, it has been shown that midseason P applications can be effective (Stark et al., 2003; Stark and Westermann, 2008; Westermann, 2005), likely due to an upright canopy architecture (high percentage of water and P and other solutes follow the stems to be deposited at the base of the plant) and an abundance of surface-feeding roots after the canopy closes and completely covers the soil. However, these in-season P applications are not as effective as when preplant P is mixed in the soil and in better contact with plant roots (Anghinoni et al., 1980a,b; Hopkins et al., 2010a,b; Sleight et al., 1984).

The rate of P fertilization was found to be 50% for banded versus broadcast applications to vegetable crops (Sanchez et al., 1990, 1991). The efficiency of banding versus broadcast is much greater at low versus high soil P test results, with about a threefold increase at low soil P, but approaching equivalent status at high. Similar findings were made for corn, winter wheat, and other agronomic crops (Barber, 1958; Peterson et al., 1981; Welch et al., 1966).

In-season P application probably should be viewed as a means of last resort or rescue and used only when tissue analysis indicates a P deficiency (Westermann and Kleinkopf, 1985). Rosen et al. (2014) suggested that in-season applications should only be supplementary to soil-incorporated P applications and only if tissue analysis shows a need. Hopkins et al. (2010a) showed that preplant P fertilization resulted in significant improvements in yield. Although there were trends for yield increase, the in-season and the split (50% preplant and 50% in-season) applications did not result in significant increases over the unfertilized control. Further work showed that, although incorporation into the soil is the best option, “rescue” in-season P applications have some merit with potato when P was underapplied prior to planting (Hopkins et al., 2010a,b,c; Westermann, 2005).

Hopkins et al. (2010b) found that in-season P application gave a slight, consistent U.S. No. 1 yield increase at all preplant P levels in the study (0, 112, 224, and 336 kg P2O5 ha−1). The response to preplant P increased steadily with rate increase, and the in-season application resulted in further increases in yield, even at the highest P rate. A similar response occurred for total yield, although the response to preplant P leveled off at the first rate of applied P. Horneck found similar results in separate trials with longer season conditions and, thus, higher yields in Oregon (Hopkins et al., 2014). Westermann (1984) found that P uptake and yields generally increased with supplemental P fertigation, although the results were mixed.

Although movement of soil P is very minimal in most cases, soluble fertilizer P can move long distances in soil, especially in soils with rapid macropore flow. Phosphorus moved to a depth of 18 cm through a loamy sand (Hergert and Reuss, 1976) and to 45 cm through a sand receiving a very high rate of irrigation (Stanberry et al., 1955). Differences in P source movement through application of P with irrigation water have been reported, with monocalcium phosphate, MAP, urea phosphate, and phosphoric acid moving downward more effectively than APP or di- and tricalcium phosphates (Lauer, 1988; O’Neill et al., 1979; Stanberry et al., 1965). Bar-Yosef et al. (1995) found no differences between broadcast and drip-injected P for sweet corn grown on sand. Carrijo and Hochmuth (2000) found that P applied in irrigation water was more effective than preplant incorporation for tomato. Instances where irrigation-applied P is more effective than broadcast likely are related to the placement of P in a concentrated form in or near to the root zone (Carrijo and Hochmuth, 2000; Mikklelsen, 1989). Application of P with irrigation can be effective if water movement through soil is adequate and the proper P source is used and placed near or in the root zone.

Direct foliar application of P has also been studied in potato. Laughlin (1962) found that 18 foliar sprays of just 11 kg P2O5 ha−1 gave a significant yield increase in potato, but not when combined with soil application of 404 kg P2O5 ha−1. However, the soil application resulted in a significantly greater yield than foliar applications alone. Other studies showed no benefit of foliar-applied P (Allison et al., 2001; Rosen et al., 2014). Although Hiller and Koller (1987) found general responses to foliar nutrition, there was no response to foliar P nutrition at any of three field locations tested.

Foliar applications have been studied in a wide variety of other crops. In general, a limited amount of P can be delivered in this fashion but not enough to meet high demand, and in many cases, there are no or there are negative responses. Teubner et al. (1962) found that multiple foliar sprays resulted in P absorption in harvested plant parts at 12% of the total need, but that yields were unaffected and total P in the plants was not increased. Upadhyay et al. (1988) found that P fertilization applied as a foliar spray was much less effective than if all P was supplied as an incorporated soil application. Silberstein and Wittwer (1951) evaluated organic and inorganic P foliar sprays on vegetable crops, finding that orthophosphoric acid was the most effective source, but the responses were very minimal and some compounds resulted in toxicity with P concentrations as low as 0.16%. However, Barel and Black (1979a,b) found that several polyphosphate and some other phosphate fertilizers could be applied at rates up to threefold greater than orthophosphate without causing leaf toxicity and that yields of corn and soybean were higher with tri- and tetrapolyphosphate than with orthophosphate. In many cases, foliar application of P along with other nutrients (N, K, S, etc.) often resulted in maturity delays and no or negative yield responses (Batten and Wardlaw, 1987; Garcia and Hanway, 1976; Harder et al., 1982a,b; Parker and Boswell, 1980; Robertson et al., 1977). In summary, timing is not a critical factor for P fertilizer application, but incorporation into the soil is relatively more efficient than canopy ground or surface applications.

Nutrient placement can increase PUE (Kissel et al., 1985; Stevens et al., 2007). Fertilization can impact P availability through at least two avenues. First, there are more microsites with readily soluble adsorbed or precipitated P. Each site increases the likelihood of a root encounter and uptake. Broadcast fertilization greatly impacts this means of P supply to plants. The other avenue is through an increase in soil solution equilibrium P level (Kissel et al., 1985; Lindsay, 2001; Sposito, 2008). A concentrated fertilizer band or point injection greatly amplifies these effects in a small zone in the soil, providing a highly soluble pool for plant uptake. Hopkins et al. (2014) showed that there is about a 60-fold increase in the bioavailable P in the center of a fertilizer band compared with when the same amount is broadcast in the bulk soil. This increase is temporary but allows plant roots to bathe in soluble P, particularly during the critical early-season growth period. Kovar and Barber (1987) used modeling to show PUE will likely increase if P banding contacts about 5% of the soil volume, especially with high P-fixing soils low in soil test P (Kovar and Barber, 1987).

For maximum effect, the fertilizer needs to be placed in an area where roots are likely to be congregated. For corn and most other species, placement generally is recommended at 5 cm to the side and 5 cm down from the seed for interception by early roots, which tend to grow diagonally for most species. Potato is similar, although placement is generally slightly further away at 7–8 cm, with a wider range of acceptable depth ranging from 7–8 above or below the seed piece (Hopkins and Stephens, 2008, 2014). Placement too far from the main root system results in little or no P uptake, especially for species with small root systems (Lesczynski and Tanner, 1976; Opena and Porter, 1999). Moorby (1978) found no P uptake from labeled fertilizer applied in the adjacent furrow or beyond for potato. Hammes (1961, 1962) found little P uptake for banded fertilizer applied below 30 cm and that the most efficient uptake occurred 5 cm to the side of the seed piece. For sugar beet, placement should be directly below the seed in order to intercept the taproot dominant in the first few weeks of growth (Hopkins and Ellsworth, 2006; Stevens et al., 2007).

It is important to understand root morphology and architecture of individual species in order to most effectively apply a concentrated fertilizer band. Usually, these concentrated fertilizer bands are applied at planting. However, in some cases, the application is applied preplant. Preplant application is especially common for potato, with the P often applied when rows are formed. In this case, it is essential that the concentrated band be placed to the side of the seed piece and deeper than the planting depth to avoid disruption of the band at planting when the soil is disturbed. It is crucial that the concentrated band of P remains intact to realize the benefit of increased P solubility (Hopkins and Stephens, 2008, 2014).

Appropriately placed fertilizer bands increase P uptake efficiency to 25%–35% (first year recovery) compared with 1%–10% if the P is broadcast applied (Hopkins et al., 2014; Kissel et al., 1985; Mattingly and Widdowson, 1958; Randall et al., 1985; Syers et al., 2008). Using radioactively labeled P, Baerug and Steenberg (1971) showed a doubling of P recovery from a concentrated band (5 cm to the side and 2 cm down from the seed) compared with a broadcast application. Although not always a replacement for broadcast fertilizer P, adding P to soil in a concentrated band often results in additional increases in potato tuber yield and quality over a single broadcast application (Hawkins, 1954; Jackson and Carter, 1976; Kelling and Speth, 1997; Kingston and Jones, 1980; Liegel et al., 1981; Soltanpour, 1969b; Sparrow et al., 1992). Banding P increases P uptake, especially for early-season growth when P availability is most limiting due to low soil temperatures and a poorly developed root system (Marschner, 2012). Hopkins et al. (2014) stated that these concentrated bands often result in increased rates of early-season shoot and root growths and higher concentrations of potato petiole P, with the consequence being gains in yield and quality. However, early-season growth boosts due to concentrated bands do not always equate to end of season yield increases, as plants can sometimes “catch-up” if the conditions and length of growing season are optimum.

Recently reported research results show an additive response if banded fertilizer P was applied in conjunction with broadcast-incorporated P for potato grown in calcareous soil (2%–12% CaCO3) with Olsen bicarbonate extractable P of 8–18 mg kg−1 (Hopkins et al., 2014). In moderately high testing soils, such as those that have received heavy manure applications over time, plants may respond to a band application even when the soil test recommends no additional P applications (Stark et al., 2004). The effectiveness of banded P for potato has been shown to vary with P source in calcareous soil (Stark and Ojala, 1989), with the pH of the fertilizer solution being a key factor. Banding also has been beneficial in low pH soils by concentrating P near the early developing root system (Rosen and Eliason, 2005).

Despite the benefits of applying P in a concentrated band, all plant roots require adequate P throughout the entire rooting zone. Although P is mobile in plants, it may not be translocated efficiently from one distant root to another. This inefficiency is because the P would have to be transported to the shoots and then back to the root with photosynthates; consequently, it is best to apply both broadcast and banded P to soils with low to medium soil test levels (Stark et al., 2004). When soil test values are high, it is generally not recommended to apply a broadcast P (Stark et al., 2004). However, there are reported incidents of responses to banded P in soils with high residual P (Hopkins and Ellsworth, 2006; Hopkins and Stephens, 2008, 2014; Rosen et al., 2014). Liegel et al. (1981) found broadcasting to be as effective as banding on two sand soils, although they did find an advantage for band application on a more coarse textured soil. Rosen et al. (2014) stated that it is essential that all of the P be banded on soils that have a high potential for P fixation.

It should be noted, however, that too much of a good thing can be bad. Hegney and McPharlin (1999) found negative results when banded P was applied in direct contact with potato seed pieces. Other species show toxicity if high rates are applied in direct contact with seeds. Plants need salts in order to regulate water uptake, and all nutrients are found in salt form. However, excessive salts desiccate plant tissues if the soil osmotic potential becomes extremely negative, particularly for germinating seeds and seedlings. Fertilizer can be applied in direct seed contact as long as the rate is not too high. Orthophosphate is a salt component, but when it is applied as a fertilizer its salt effect is minimal because the majority is quickly precipitated into solid forms. As such, its direct impact on salt concentration is less than more soluble nutrients, such as N and K. Thus, P can be directly applied to seed relatively more safely than other nutrients, although accompanying cations are often soluble salts. To be safe, no fertilizer should be applied in direct seed contact without research showing that the rate applied is acceptable for the species and soil and environmental conditions. Note that because salt damage is a function of soil moisture status, dry soil conditions are relatively more likely to result in salt damage to plants. Furthermore, small seeded species tend to be more readily impacted by salts in close proximity to the seed or seedling than species with large seeds.

3.10.5  Best Management Practices Impact Fertilization

As P is poorly soluble and immobile in the soil, any factor that increases root growth should expose the plant to more P for absorption. Miller and Hopkins (2007) and Hopkins et al. (2007a) reviewed best management practices (BMPs). In general, these BMPs can be applied across crops and conditions, but specific circumstances call for specific practices. One BMP that is especially important is to avoid root damage due to tillage, insect and pathogen damage, herbicides, salt, or other toxicities to promote a healthier root system, which can greatly enhance P uptake.

In summary, P nutrition in plants has been a major contributor to societal success in the last two centuries. It is vital to understand its essential role in plants and their difficulty in obtaining it from soil, with wide differences observed across species and growing conditions. Tissue and soil analysis tools greatly help in guiding the management of P nutrition in plants. As a society, we need to follow BMPs for the growing of plants and P fertilization to sustain crop productivity simultaneously with improving environmental quality and resource conservation. Ample, but not excessive availability of water and nutrients is also important.

3.10.6  Environmental Issues

Despite the many positive roles of P, not long after its widespread use, it became known that it is an environmental contaminant (Ruark et al., 2014). In the United States, the Environmental Protection Agency (EPA) has declared that more than one-third of all water bodies are impaired with P pollution. The problem is related to water quality from point and nonpoint sources (Romkens et al., 1973; Ryden et al., 1973). Point source pollution occurs primarily from P-rich municipal and industrial wastes being dumped into surface water bodies. Even when treated to remove pathogens and other hazards, P typically has not been removed. However, even if all of the P was removed from point sources, nonpoint source contributions are massive and very difficult to identify and treat.

The problem with P entering surface water is related to nutrient enrichment (Ruark et al., 2014; Sharpley et al., 1999). Algae and other aquatic organisms are like land plants, needing P and other nutrients. In most freshwater systems, P is the primary limiting factor for algal growth. When these simple organisms are fertilized with nutrient-rich pollution, their yields increase similarly to what happens with more complex land plants when the most limiting factor for growth is overcome (Correll, 1998; Schinder, 1977). Therefore, when adequate sunlight and heat are present, algal blooms occur. By themselves, the population of algae can be unsightly and odoriferous and can interfere with recreation and aquatic-based industries. However, the most serious problem occurs upon the death of the algae. The microbes responsible for decomposing the algae also require nutrients, including O2. In some cases, their population exceeds the carrying capacity of the water body as they deplete it of O2 and create a hypoxic condition (Correll, 1998; Daniel et al., 1998). This condition can result in the broadscale death of fish and other aquatic organisms, which also require O2, again causing unsightly and odoriferous problems, as well as negative impacts on fishing and other related industries and recreational activities. In addition to algal growth, eutrophication can result in cyano-bacterial blooms as well and can result in poor palatability of the water for drinking and livestock and human health hazards (Kotak et al., 1993; Lawton and Codd, 1991). There are many reviews examining losses due to P pollution (Buczko and Kuchenbuch, 2007; Chien et al., 2011; McDowell et al., 2001; Ryden et al., 1973; Sharpley et al., 1993; Shi et al., 2011; Withers and Jarvie, 2008).

This increasing problem in recent years has prompted regulations and guidelines regarding P levels in surface waters and for practices to reduce P loading of water bodies. Ruark et al. (2014) stated that no official U.S. standard has been set for P loading to freshwaters; however, USEPA established the criterion of 0.001 mg total P L−1 for marine and estuary water (Parry, 1998). The state of Florida has adopted this same guideline for freshwater systems (Daniel et al., 1998). Other states have established a critical maximum for P, such as 0.05 mg total P L−1 in streams that enter lakes and 0.1 mg L−1 for total P in flowing waters (Ruark et al., 2014). Although the total P losses from agricultural fields are generally small compared with the total P in the soil, concentrations as low as 0.02 mg P L−1 can cause eutrophication (Correll, 1998; Sawyer, 1947; Sharpley et al., 1999; USEPA, 1996).

Point sources are easily identified and cleaned of P using the solubility principles known for soils to precipitate out the P for removal, although costs of doing so can be prohibitive. Nonpoint sources of P are much more difficult to identify and prevent. There are natural systems, as well as a variety of anthropogenic P sources, that result in P loading. However, agriculture is identified as the largest contributor of nonpoint source P loading into water bodies.

Phosphorus-enriched soils from application of traditional and, mostly, manure P fertilizers are the major source of the nonpoint problems. Organic P is much more mobile in soil than inorganic sources (Hannapel et al., 1964). The typical scenario is that crops are harvested from a wide- ranging geographical area and transported to concentrated animal operations. These feedstuffs are fed to the animals, with their wastes accumulating. These manure wastes generally are applied back to the land but are not transported back to where they came due to high transportation costs, which society, to this point, is unwilling to pay as a part of the cost of the food and fuel consumed. So, instead, the land immediately surrounding these concentrated animal facilities tends to become oversupplied with nutrient wastes.

Phosphorus moves from land to water via various mechanisms (Sharpley et al., 1994). Although not common, P concentration can become so high in soil that the equilibrium concentrations are atypically high. This action results in movement through the soil where P can enter subsurface water systems and drains (Brye et al., 2002; Eghball et al., 1996; Hansen et al., 1999; Kleinman et al., 2003; Mozaffari and Sims, 1994). Ruark et al. (2014) stated that while surface runoff is historically considered the dominant pathway by which P is transported from land to water, subsurface flow can be an important pathway in certain landscapes (e.g., sandy soil; well-structured, fine-textured soils with well-defined macropores; and porous organic soils with low P-sorption capacities). They also stated that subsurface movement of P is dominated by preferential flow via macropores exacerbated by the presence of artificial drainage such as tile drainage.

However, most of the P transport is a surface phenomenon. P tends to accumulate at the soil surface and, as such, precipitation events that result in overland flow of water tend to pick up soluble P, which is transported to surface water. The quantity of P transported as dissolved P is a function of desorption–sorption and dissolution–precipitation reactions that cause P to exist in soil solution (Sharpley et al., 1993, 1994). Ruark et al. (2014) stated that transport of dissolved P movement is a function of the factors that cause surface runoff to occur (e.g., slope, surface roughness, and residue cover).

Another mechanism of P movement to surface water is due to transport of P adsorbed to soil and mineral solids via wind and water erosions. Ruark et al. (2014) cited several sources that show an average of 86% attributed to particulate P movement. Researchers found during year-round monitoring of fields in Wisconsin that, whereas the median annual dissolved and sediment-bound P losses were similar, the maximum annual particulate P loss was five times greater than maximum dissolved P loss, due to erosion with spring precipitation (Good et al., 2012).

Areas that tend to have P-enriched water bodies have an abundance of animals per unit land area along with high precipitation rates. Steep slopes and nonvegetated soils are more prone to offsite P movement through water and soil transport. Proximity to water is also a factor, with manure or fertilizer P applied to a soil close to a water body much more likely to be deposited in water than if applied further away.

Practices to control P losses target the reduction of P available for loss (source management) and reduction of movement of P to a water body (transport management) (Ruark et al., 2014; Sharpley et al., 1994). Ruark et al. (2014) stated that concerns relative to source management include (1) soil test P levels, (2) rate and manner of P applied, and (3) rate and implementation of BMPs (Daniel et al., 1998; Eghball et al., 2000; Ginting et al., 1998; Sharpley et al., 1994). The most obvious strategy is to avoid the excessive application of manures and fertilizers. Many areas have passed laws for farmers and even homeowners with regard to manure and fertilizer applications. The Natural Resource Conservation Service (NRCS) has offered various financial incentives to growers to implement strategies to prevent P pollution. One example of how this action has impacted agriculture is that there has been an influx of dairy operations into western states of the United States where soils have a high capacity for P fixation, precipitation is low, and water bodies tend to be further away from farm fields. For example, dairy and cattle productions recently have surpassed potato as the main source of agricultural income in Idaho. Moving operations to other locales is more financially agreeable than is paying to transport manure long distances, although transport is another strategy that can be employed to avoid the accumulation of P in soils.

Several studies show a positive correlation between concentrations of P in soil tests and in runoff water (Andraski and Bundy, 2003; Cox and Hendricks, 2000; Pote et al., 1996, 1999; Sims, 1998). Andraski and Bundy (2003) concluded that traditional soil P tests are effective for predicting the risk of P loss, although the relationship is not perfect (Cox and Hendricks, 2000; Daniel et al., 1993; Hart et al., 2004; Sharpley, 1995). There has been a trend for increasing levels of soil P in some locales due to P applications in excess of crop need (Bundy and Sturgul, 2001; Sharpley et al., 1994, 2001). A survey of 1928 farms in Wisconsin revealed that 80% applied excessive P to corn (Shepard, 2000). However, Bundy and Sturgul (2001) stated that, although excessive application continues, the trend is in decline. The Bray P1 soil test concentrations increased from 34 to 51 mg kg−1 between about 1970 through the late 1990s, but then stabilized. The International Plant Nutrition Institute (IPNI, 2011) also reflects this trend, with some locales decreasing in soil test P. However, soil P is especially an issue in locales with an abundance of farm manure (Ginting et al., 1998; Shepard, 2000; Sims, 1998).

Ruark et al. (2014) stated that having a high test for P in soil is not enough alone to cause eutrophication of nearby water bodies. Conditions must exist where P is transported easily, especially steep slope and close proximity to water (Sharpley et al., 1992; Sims et al., 2000). As particulate P is the main source of contamination of waters, efforts to control soil erosion are the primary focus [e.g., soil type, slope, distance to surface water, crop management, conservation practices, and intensity, timing, and duration of rainfall (Gburek et al., 2000; Hart et al., 2004; Hudson, 1995; Kimmell et al., 2001; McDowell et al., 2001; Sharpley et al., 2001)].

There have been significant efforts in the United States to develop P indexes to help prevent P pollution (Sharpley et al., 2003). The P indexes tend to factor in the aforementioned soil-loss risk factors, along with bioavailable P concentration in soil. It is recommended that soils in close proximity to water, especially those that are on steep slopes, should not receive manure applications and that P fertilizer should be applied carefully and judiciously. Soils that have low soil test P can accept manure or fertilizer P applications without much risk of loss, especially if incorporation takes place. Keeping a soil vegetated greatly decreases the risk of P transport as soil erosion is much more likely to occur when soil is void of plant growth. Similarly, vegetated buffer strips between farm fields and water bodies can be used to capture soil and P in water runoff. Incorporating P into the soil can reduce the surface concentration of P, but there is a temporary increase in risk due to exposure of bare soil to the forces of erosion.

Ruark et al. (2014) stated that fields with the highest risk for P loss are those with both source and transport factors, that is, those with high P additions or soil test P and are coincident with high relative transport risk (surface runoff, erosion, and/or subsurface flow). If a site has high soil test P or high amounts of nutrient addition from manure or fertilizer but is not located near a lake or stream, the risk for P loss to water is much less. Likewise, if a field is located next to a stream but has low levels of soil test P, risk for P loss is also low.

Fortunately, there seem to be reasonable solutions to avoid problems of P pollution in most circumstances (Daniel et al., 1998; Sharpley et al., 1994, 2001; Sims et al., 2000). For most crops, the level of soil test P that is considered optimum for production and for which no added P is needed is well below that of where there is a high risk of P transport. The exception to this rule is our unique potato species. The problem has been discussed previously and is reviewed thoroughly by Ruark et al. (2014), who give an excellent review of P pollution and the unique problems with potato. Essentially, the issue is that potato, unlike most all other species, continues to respond to P fertilization at high and even exceptionally high soil test levels. In some cases, potato grown in high-rainfall areas with soil test levels that are very high may still require P applications. Furthermore, typical potato production results in the soil remaining bare for relatively longer periods of time than for most other crops. The soil receives deep tillage in the fall or early spring in order to create friable soil conducive to tuber growth, and then the planting, hilling, and harvesting operations all involve near complete turning over of the soil. These four operations result in bare soil exposure that, along with very slow early-season growth, give extremely high susceptibility to P transport by wind and water erosion of soil. However, Ruark et al. (2014) also stated that there is minimal research on P pollution from potato fields and that the risks may not be as great as suggested here. The bottom line is that potato production in high-rainfall areas in close proximity to water bodies is very problematic with regard to P pollution risk.

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