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The Global Phosphorus Cycle: Past, Present, and Future

^* Department of Earth Sciences
Indiana University-Purdue University Indianapolis (IUPUI)
723 West Michigan Street, Indianapolis, IN 46202, USA
E-mail: gfilippe{at}iupui.edu

	ABSTRACT

TOP ABSTRACT IMPORTANCE OF PHOSPHORUS--WHY P? THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE:... REFERENCES

 
The cycling of phosphorus, a biocritical element in short supply in nature, is an important Earth system process. Variations in the phosphorus cycle have occurred in the past. For example, the rapid uplift of the Himalayan-Tibet Plateau increased chemical weathering, which led to enhanced input of phosphorus to the oceans. This drove the late Miocene "biogenic bloom." Additionally, phosphorus is redistributed on glacial timescales, resulting from the loss of the substantial continental margin sink for reactive P during glacial sea-level lowstands. The modern terrestrial phosphorus cycle is dominated by agriculture and human activity. The natural riverine load of phosphorus has doubled due to increased use of fertilizers, deforestation and soil loss, and sewage sources. This has led to eutrophication of lakes and coastal areas, and will continue to have an impact for several thousand years based on forward modeling of human activities.

KEYWORDS: phosphorus, biogeochemistry, soil, cycling, paleoclimatology

	IMPORTANCE OF PHOSPHORUS—WHY P?

TOP ABSTRACT IMPORTANCE OF PHOSPHORUS--WHY P? THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE:... REFERENCES

 
Nature apparently made an odd choice when it chose to build most of the critical photosynthesis and metabolic pathways around phosphorus (Westheimer 1987). Phosphorus (P) is present in only minute quantities in Earth's crust (0.09 wt%). It is interesting to note that P is twice as abundant in Martian rocks (Greenwood and Blake 2006). Once P is liberated from minerals during weathering, it is quickly sequestered into a number of more recalcitrant phases, limiting its day-to-day accessibility to plants and organisms. Phosphorus has no stable atmospheric gas phases, so unlike the case for other critical bionutrients, such as nitrogen and carbon, ecosystems have to depend on aqueous transfer of this nutrient. The only exceptions are completely P-depleted ecosystems. Examples include transport-limited regimes such as the Amazon Basin, and old volcanic islands like Kauai (e.g. Kurtz et al. 2001) where ecosystem survival depends on the minute amount of P that is delivered by trans-Pacific dust. In summary, there simply is not much P around, it does not travel well, and it is not readily bioavailable.

In spite of these limitations, P plays an essential role in biological systems. We and all other vertebrates owe our gravity-defying skeletons to the hydroxylapatite that makes up bones (for more on P mineral chemistry, see Oelkers and Valsami-Jones 2008 this issue). We also depend on hydroxylapatite (with carbonate and fluoride substitution) to make our teeth strong enough to bite into a crispy apple. Growing that apple, in turn, depended on the Calvin cycle photosynthetic pathway and the important role that adenosine triphosphate (ATP) plays in this cycle. The double helix of our DNA is only possible because of the phosphate ester bridges that bind the helix strands. All cells owe their very structure to the phospholipids that make up cell wall membranes. Earth's biological systems have depended on P since the beginning of life (e.g. Nealson and Rye 2004), and we have no reason yet to doubt that P is critical to all biological systems in the universe. The unique energetics of the phosphate molecule are central to the function of ATP, the linchpin for metabolism in biological systems. ATP is the most abundant biomolecule in nature (Schlesinger 1997).

Phosphate hydrolyzes only slowly in the absence of enzymes. It is very stable at the pH of cell interiors, but it hydrolyzes rapidly when enzymes are present. Phosphate mobility within organisms is high, and thus in contrast with environmental conditions, phosphate is readily available within biological systems. Finally, P is the essential ingredient in bone, contributing to a hydroxylapatite/organic scaffold that has strength, some flexibility, an open structure for substitution of some essential nutrients, and a biologically friendly dissolution and precipitation behavior, i.e. it rapidly dissolves and precipitates when solution composition is right (Skinner and Jahren 2004). Thus, in spite of low natural abundance, the chemical behavior of phosphate makes it the most likely candidate around which to build biological systems.

In this paper, I explore the sources, interactions, and eventual fate of P on Earth from the system perspective. I also outline efforts to understand variations in P cycling, with a look both forward and backward through time. As we have gained more and more understanding of various aspects of global P cycling, we have put some debates to rest and have sparked others. But one aspect has remained constant: an understanding of the P cycle is critical to our understanding of biological, chemical, and geological cycles on Earth and beyond, so it will likely continue to be an active research topic for decades to come.

	THE GLOBAL PHOSPHORUS CYCLE IN THE CONTEXT OF THE PREHUMAN ERA

TOP ABSTRACT IMPORTANCE OF PHOSPHORUS--WHY P? THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE:... REFERENCES

 
Phosphorus is present at an appreciable concentration in only a few minerals. The main P-bearing mineral in igneous rocks is fluorapatite, an early-formed accessory mineral. It appears as tiny, euhedral crystals associated with ferromagnesian minerals. In sedimentary rocks, P is typically associated with authigenic carbonate-fluorapatite (CFA; more on this later). All apatite minerals contain phosphate oxyanions linked by Ca²⁺ cations to form a hexagonal framework, but they contain different elements at the corners of the hexagonal cell.

View larger version (21K): [in this window] [in a new window]   FIGURE 1 Modeled changes in soil phosphorus availability with time (after Filippelli 2002), showing transformation of mineral phosphorus into non-occluded (i.e. highly labile) and organic forms before eventual dominance of occluded (oxyhydroxide-bound) and organic forms. The bioreactivity of phosphorus increases from mineral to occluded to organic forms. Note that phosphorus is continuously lost from the system.

In soils, weathering releases P from minerals by several processes. First, biochemical respiration releases CO₂, increasing acidity around degrading organic matter and root hairs; poorly crystalline P-bearing minerals dissolve rapidly in this acidic environment, releasing P to root pore spaces (e.g. Schlesinger 1997). Second, organic acid exudates from plant roots also can dissolve apatite and release P to soil pore spaces (Schlesinger 1997). Upon dissolution, P is transformed by several processes into forms that are less immediately bioavailable. It can be incorporated into plant tissue where it is converted into an organic form. Plants actively incorporate phosphate to form biomolecules critical to photosynthesis and metabolism. Plants have developed several tactics to increase the supply of P to roots, including the secretion of phosphatase, an enzyme that can release bioavailable inorganic P from organic matter into soil pore spaces (Bucher 2007). The symbiotic fungi mycorrhizae can coat plant rootlets, excreting phosphatase and organic acids to release P and providing an active uptake site for the rapid diffusion of P from soil pore spaces to the root surface. In exchange, the plant provides carbohydrates to the mycorrhizal fungi (Smith et al. 2003). When plants or tissues die, organically bound phosphorus undergoes the same fate as organic litter; bacterial and fungal reactions in soils progress slowly, oxidizing organic matter and releasing P as phosphate to soil solutions (Bucher 2007).

An additional sink for P released by weathering is iron and manganese oxyhydroxides, where P is either co-precipitated with them or adsorbed onto their surfaces during soil weathering. These reducible Fe and Mn species are termed "occluded" fractions in soils. They have a large binding capacity for phosphate because of their extremely high surface area and their overall positive charge (Filippelli 2002). These P-bearing phases often constitute the main, long-term storage pool for soil P. The labile (unstable) forms include P in soil pore spaces (as dissolved phosphate ion) and adsorbed onto soil particle surfaces (these forms are termed "non-occluded"), as well as P incorporated in soil organic matter. On a newly exposed rock surface, nearly all of the P is in apatite. With time and soil development, however, it is released and incorporated in other phases (FIG. 1; Filippelli et al. 2006). Over time, the total amount of P available in the soil profile decreases, as soil P is lost through surface and subsurface runoff (e.g. McDowell and Sharpley 2001). Eventually, the system reaches a terminal steady state, in which soil P is heavily recycled and any P lost through runoff is balanced by new P weathered from apatite at the base of the soil column.

Transport from Land to Sea
Transport of eroded soil by rivers delivers P to the oceans. Riverine P is in two main forms: particulate and dissolved. Most of the particulate P in rivers is held within mineral lattices and never participates in the active biogenic cycle. This is also true after delivery to the oceans, because dissolution rates in seawater, where pH is high and ionic buffering is strong, are exceedingly low. Thus, much of the P physically eroded from continents is delivered relatively unaltered to the oceans, where it is sedimented on continental margins and in the deep sea, waiting for subduction or accretion to give it another chance to participate in the continental P cycle. Some P-bearing particulate is adsorbed onto the surfaces of other soil particles, some P is held within soil oxyhydroxides, and some is incorporated into particulate organic matter. The fate of organic P after transfer to the ocean is poorly understood. For example, P adsorbed onto soil surfaces may be effectively removed in response to the high ionic strength of ocean water, providing an additional phosphate source to the ocean. A small amount may be released from terrestrial organic matter during bacterial oxidation after sediment burial. Finally, some sedimentary environments along continental margins are suboxic or even anoxic, conditions that favor oxyhydroxide dissolution and release of sorbed P. Several important studies have examined the transfer of P between terrestrial and marine environments (e.g. Ruttenberg and Goñi 1997), but quantification of the interactions between dissolved and particulate forms and the aquatic/marine interface is lacking.

Marine Cycling
Once in the marine system, dissolved P is a limiting nutrient for biological productivity (e.g. Ammerman et al. 2003) and is perhaps the ultimate limiter of ocean productivity on geologic timescales (Tyrrell 1999; Bjerrum and Canfield 2002). Phosphorus concentrations follow the nutrient profile in the ocean, with surface depletion and deep enrichment. Concentrations are near zero in most surface waters, as P is taken up by phytoplankton as a vital component of their photosystems. In deep water, phosphate concentration increases with water age, so values in the young, deep waters of the Atlantic are 40% lower than those in the older Pacific Ocean. Once P is incorporated into organic matter, it follows a similar biogeochemical route as the organic matter itself, undergoing active recycling in the water column and at the sediment-water interface. Several recent examinations of P cycling and recycling (e.g. Benitez-Nelson 2000; Paytan and McLaughlin 2007) elucidate the process in which organic P in the water column is transferred from organisms to dissolved inorganic forms and back to organisms.

View larger version (33K): [in this window] [in a new window]   FIGURE 2 Percent of total reactive P in authigenic and organic phases for (A) the anoxic Saanich Inlet (ODP Site 1033) and (B) the deep-sea eastern equatorial Pacific (ODP Site 846). This comparison reveals the sink-switching that occurs during sedimentary P cycling, with the growth of an authigenic P phase and loss of P from organic phases with age and depth.

	THE GLOBAL PHOSPHORUS CYCLE IN THE PAST: A RECORD OF GLOBAL CHANGE

TOP ABSTRACT IMPORTANCE OF PHOSPHORUS--WHY P? THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE:... REFERENCES

 
Perhaps the most important questions to ask about the marine P cycle include how it has varied in the past, what has driven this variation, and how this has affected other biogeochemical systems. Although simple to ask, these questions are very difficult to answer when viewed through the filter of the geologic record. For example, the most recent paradigm for the episodic nature of large marine deposits rich in P, called phosphorites and typified by the massive Permian Phosphoria Formation of the western US, was that these deposits reflect times in Earth's history when the transport of P from continental weathering to the ocean was significantly higher than it is today. What had not been recognized in this argument was that phosphorite deposits are the result of intervals of "normal" marine organic matter deposition in regions of high biological productivity on continental margins and that P accumulation rates were similar to those of today. Deposition was followed by intervals of significant sediment reworking (often in response to sea level variations) and concentration of the disseminated P into phosphatic lags and hard grounds. An example of a high-P sedimentary rock from the Miocene Monterey Formation is presented in FIGURE 3. When this process repeats itself many times, the result is a thick accumulation of P-rich rock such as the Phosphoria Formation, which certainly represents a unique sedimentary environment but not necessarily a unique, global P-cycling event. This is not to say that the global P cycle remains constant over time. On the contrary, global P cycling varied in the past, and below are two examples.

View larger version (98K): [in this window] [in a new window]   FIGURE 3 Phosphatic shales from the Miocene Monterey Formation, Shell Beach, central California, USA. The black shales are rich in organic matter, with up to 15 wt% total organic carbon (Filippelli 1997b), and are marked by whitish tan laminae and nodules of nearly pure carbonate-fluorapatite. These are seen clearly in the sliced section on the bottom right; scale is 2 cm. These phosphatic shales may be the result of minor reworking, but they are the raw materials for economically significant phosphorite deposits. Approximate height of top two images is 60 cm.

View larger version (97K): [in this window] [in a new window]   FIGURE 4 Some parts of Tibet are still experiencing rapid uplift and physical erosion, as seen in this photo taken near Tingri, China. Several episodes of rapid erosion have produced high-energy braided channels and a recent river terrace (covered by rice paddies) that has been downcut by the modern river (PHOTO BY G. FILIPPELLI).

View larger version (25K): [in this window] [in a new window]   FIGURE 5 Geochemical record from marine sediments, showing dramatic transient shifts in P accumulation rate, Ge/Si in opaline silica, and carbon isotope composition (bulk marine carbonates) in the interval from just before 8 Ma to 4 Ma; this interval coincides with the intensification of the Asian monsoon (ORIGINAL DATA SOURCES IN FILIPPELLI 1997A).

Glacial-Interglacial Variations in the Oceanic P Cycle
What role does sea level change play in the marine P mass balance? This is an important question, given observed variations in shelf area caused by eustatic sea level changes on glacial timescales. The gain and loss of a sedimentary sink that is small in area but large in terms of net accumulation and biogeochemical dynamics certainly should play a role in whole-ocean geochemical budgets. The shelf-nutrient hypothesis (Broecker 1982) states that the loss in continental margin sinks for nutrients and carbon during glacial sea level lowstands (which resulted in a decrease in continental margin area of 60% during the last glacial maximum compared to now) should result in a net transfer of these components to the deep-ocean sink. The consequence would be significantly different and climatically mediated deep-ocean budgets for these elements. Many aspects of the shelf-nutrient hypothesis have been tested and debated, but little has been done to directly examine P budget changes in the ocean for this period.

View larger version (14K): [in this window] [in a new window]   FIGURE 6 Changes in the mass balance of phosphorus on glacial timescales interpreted from the marine record of phosphorus burial (P/Ti), compared to a sea-level-based model (using the marine oxygen isotope record of ice volume) of phosphorus mass balance changes due to the redistribution of phosphorus from exposed continental margins during glacial sea level lowstands (after Filippelli et al. 2007). The P/Ti record is a composite of individual P/Ti records from the Southern Ocean and the equatorial Pacific Ocean (Filippelli et al. 2007). Note that the quantitative transfer of nutrients from continental margins recorded by the P/Ti record is best matched by the nutrient model with a 20 ky lag; thus the net impact of redistribution of marginal nutrients to the deep sea matches with the predictions of the P response time in the ocean.

Together, this new evidence highlights the potential impact that loss of the continental margin sink could have on oceanic P cycling, suggesting that this loss should be observable in deep-ocean records. In fact, we have recently demonstrated a profound change in the P mass balance at two widely separated areas: the southeastern Atlantic sector of the Southern Ocean and the eastern equatorial Pacific over the past 400 ky (Filippelli et al. 2007). Using a number of productivity proxies (including P accumulation rates, P/Ti as a reflection of "excess" P, and nanofossil accumulation rates), we observed broad peaks in enhanced productivity (FIG. 6). Each peak began during a glacial interval, reached a maximum just after the glacial-interglacial transition, and then decreased to a low value by the beginning of the next glacial interval. These records indicate that relatively high "excess" P export occurred about 40-60 ky after the onset of glacial intervals.

At face value, this result conflicts with the shelf-nutrient hypothesis given the lag in P response, but if the residence time of P in the ocean (10-20 ky) and mass balance laws are considered, this lag is predictable. We developed a simplistic model of the deep-sea response to addition of nutrients from the exposed continental shelf during lowered sea levels using sea level records (from oxygen isotope records of global ice volume) compared to the average P/Ti value of Southern Ocean and equatorial Pacific records (FIG. 6). The deep-sea nutrient model provides an extremely good fit to the composite P/Ti record with a 20 ky lag. Two remarkable aspects of these comparative records emerge from this analysis. First, even a simple comparison of excess P export results in a reasonable fit to a deep-sea nutrient model based on global sea level variations alone (FIG. 6). Second, the 20 ky lag, which provides the best long-term fit to the P/Ti data, is what would be expected given the P response time in the ocean as currently estimated (between 10 and 20 ky).

The shifts in the oceanic P mass balance supported by these deep-ocean records have several important implications for global ocean productivity variations and carbon cycling. First, changing the depositional sink of P from the high sedimentation rate/short water column continental margins to the low sedimentation rate/deep water column deep-sea basins during glacial periods would enhance the degree of P recycling from particulate to dissolved material both in the water column and at the sediment-water interface, thus increasing the inventory of dissolved P in the oceans. Second, if the phosphate inventory is in fact increased during and just after glacial events, observed increases in surface-water productivity would not necessarily be the result solely of increased wind-driven upwelling. They could perhaps be caused by the same rate of water upwelling, but with an increased phosphate concentration. At this initial stage, the paleoceanographic P records provide deep-sea support for the "shelf-nutrient hypothesis" and should spur continued examination of geochemical mass balance variations through time.

View larger version (121K): [in this window] [in a new window]   FIGURE 7 (A) Reconstruction and projections of anthropogenic phosphorus delivered to the oceans as a result of several processes, including fertilization, deforestation and soil loss, and sewage. The projection is based on reports of population and arable land published by the World Health Organization and the Intergovernmental Panel on Climate Change. The fertilizer drop off coincides with the depletion of known P reserves. The total integrated anthropogenic input of P (1600-3600 AD) is 1860 Tg. (B) A chalky, whitish blue bloom of marine algae called coccolithophoridae off Brittany, France; the bloom is the result of excess surface-water nutrients (eutrophication). Although coccoliths are small (micrometer scale), they often form large, concentrated blooms that are visible from space. PHOTO COURTESY OF NASA

	THE GLOBAL PHOSPHORUS CYCLE: THE PRESENT AND FUTURE

TOP ABSTRACT IMPORTANCE OF PHOSPHORUS--WHY P? THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE:... REFERENCES

The human-era terrestrial P cycle, therefore, is substantially different from the prehuman cycle. This is demonstrated by the high loads of dissolved P in rivers, which are estimated at about twice natural values, and the higher loads of P-bearing particulates. Together, the net input of dissolved P from land to the oceans is 4-6 Tg P/y. This value represents a doubling of prehuman input fluxes, which clearly has led to eutrophication in coastal areas, and probably also has contributed to enhanced biological production in the whole ocean (FIG. 7B). One likely scenario is for the ocean to achieve a new steady state, in which the P output flux and the oceanic P reservoir will both increase in response to higher inputs. This new steady state would be short-lived, however, given the limited sources of P available for human exploitation and the relatively long residence time of P in the ocean. Nevertheless, a projection of anthropogenic increase to the ocean indicates that a sustained and significant eutrophication can be expected over the next two millennia (FIG. 7A). This projection does not predict global human extinction at 3600 AD (although it does not preclude it either); rather, the figure indicates the time at which projected global P resources for fertilizers will be depleted. Man will doubtless search for, and find, other avenues for recycling or concentrating P for fertilizer as the currently known resources become depleted, but these other sources will be much more limited in quantity and will not contribute "new" anthropogenic P to the system. Thus they do not impact a projection such as that shown in FIGURE 7A.

Eutrophication will impact the global carbon cycle, but will probably do little to offset anthropogenic carbon emissions. Based on the projection of P input to the ocean (FIG. 7A), the total excess input from 1600 to 3600 AD is 1860 Tg P. Given that, in the marine environment, between 106 and 170 units of C are buried per unit of P (Colman and Holland 2000), one can predict that excess phosphorus would effectively bury 76,000 to 123,000 Tg C. In essence, this burial removes C from the atmosphere through the biological fixation of carbon dioxide during photosynthesis. The present annual rate of anthropogenic C addition to the atmosphere is 7900 Tg C (Marland et al. 2007), so the P eutrophication effect would only account for about 10-15 years of anthropogenic carbon emissions to the atmosphere over the next 2000 years (i.e. only 0.6% of total projected carbon emissions, if emissions stay constant). Although the net effect as a carbon sequestration mechanism is minimal, the ecological impact of P fertilization to the ocean could be extreme. Given the other assaults on marine ecosystems, including warming and acidification of surface ocean waters from higher carbon dioxide levels, it would be pure speculation to project how P eutrophication would affect ecosystem structure and distribution in the future. However, those who have witnessed local eutrophication in ditches, streams, ponds, and lakes can attest to the ecological devastation that excess nutrients and the proliferation of monocultures can cause in such isolated environments. The eutrophication of coastal and open-marine ecosystems would result in a grim future for ecological diversity.

	ACKNOWLEDGMENTS

 
I acknowledge support from the National Science Foundation, the donors to the Petroleum Research Fund (administered by the American Chemical Society), and the Ocean Drilling Program. I also acknowledge discussions with many colleagues over the years on the topic of phosphorus cycling, and I thank Eric Oelkers, who encouraged the writing of this article, and several critical reviewers, who helped to improve it.

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TOP ABSTRACT IMPORTANCE OF PHOSPHORUS--WHY P? THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE... THE GLOBAL PHOSPHORUS CYCLE:... REFERENCES

 

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