The Phosphorus Cycle

1. The Phosphorus Cycle Jen Morse morsej@caryinstitute.org 10 January 2013

2. Is the Phosphorus Cycle important? • Global P cycle in Schlesinger 1997: 3 pages (vs 13 for N) • Terrestrial P cycling in Chapin 2002: 4 pages (vs 18 for N) • Phosphorus cycling is: • A) Simple • B) Boring • C) Not important

3. Questions to consider • What makes phosphorus important? • Phosphorus cycling: • How does global cycle P differ from N? • Forms, pools, fluxes • P cycling in soils vs. inland waters vs. marine systems • Controls on availability & interactions with other elements • Why care about ecosystem P inputs and losses?

4. Biological importance of PEnergy and evolution • DNA, RNA • ATP  energy transformations • Phospholipids  cell membrane structure • Bones and teeth of vertebrates ATP DNA

5. Phosphorus basics: • 11th most abundant element on land, 13th in seawater (Smil 2000) • Elemental P: highly reactive • Isolated from urine by Hennig Brandt in 1669 • Glows and spontaneously reacts: alchemy... matches... explosives • Only 31P is stable; radioisotopes include 32P,33P • Stable isotope ecology methods don’t apply for P

6. Calliergon giganteum. Photo by F. R. Wesley.

7. P has similar oxidation states to N... R-NH2, NH4+ NO3- NO2- NO N2O N2 +2 +5 +3 +1 0 -3 PO43- (inorganic), P(=O)(OR)3 (phosphate esters) P(OR)3 (phosphite esters) Elemental P (highly reactive) PH3(phosphine) +2 +1 +5 +3 0 -3 ... but no critical redox transformations or significant gas phase.

8. Questions to consider • What makes phosphorus important? • Phosphorus cycling: • How does global cycle P differ from N? • Forms, pools, fluxes • P cycling in soils vs. inland waters vs. marine systems • Controls on availability & interactions with other elements • Why care about phosphorus inputs and losses?

9. Nutrient inputs Internal cycling Ecosystem Nutrient losses Chapin et al. (2002)

10. Chemical weathering of rocks • Biological fixation • Deposition from atmosphere • Fertilizers • Transfer of nutrients • Between plants/primary producers and soil/benthos • Between organic and inorganic forms • Changes in ionic forms • Biological uptake • Interactions with mineral surfaces • Leaching • Trace gas emissions • Wind and water erosion • Fire • Harvest Nutrient inputs Internal cycling Ecosystem Nutrient losses Chapin et al. (2002)

11. Chemical weathering of rocks • Biological fixation • Deposition from atmosphere • Fertilization • Transfer of nutrients • Between plants/primary producers and soil/benthos • Between organic and inorganic forms • Changes in ionic forms • Biological uptake • Interactions with mineral surfaces • Leaching • Trace gas emissions • Wind and water erosion • Fire • Harvest P inputs Internal cycling Ecosystem P losses Chapin et al. (2002)

12. N most abundant in atmosphere... (N fluxes in Tg/yr) Chapin et al. (2002) Fig. 15.4

13. ... most P stored in soils, sediments, ocean (P fluxes in Tg/yr) Chapin et al. (2002) Fig 15.6

14.  P becomes available at LONG time scales Thousands to millions of years Decades, Accelerated by human activities

15. Biologically available P is limited by parent material and supply • Relatively scarce (localized) in mineral form, low solubility in water • Ultimately tends to limit production: • In aquatic systems • Terrestrially at long time scales Bennett & Schipanski (2013) redrawn from Walker & Syers (1976) and Vitousek et al. (2010)

16. Nutrient limitation during ecosystem development Fertilization experiment: Hawai’ian tree diameter across chronosequence plots Younger soils more N-limited Oldest soils more P-limited (but co-limitation is important) Model applies to terrestrial ecosystems: Tropics vs. temperate zones Vitousek & Farrington (1997)

17. Atmospheric P inputs • Sources: • Arid lands in Asia and N. Africa • Deposition zones: • *highly weathered, humid tropical forests • Amazon • Caribbean • Congo • *Open ocean

18. P cycling in soils High pH biota Ca-P (soil solution) Active SOM Fe/Al-P Low pH Passive Adapted from Brady & Weill (1999) INORGANIC P ORGANIC P

19. Mineral P forms in soils Fixation by hydrous oxides of Fe, Al, and Mg Brady & Weill (2001)

20. Sources of P in soils: Weathering Ca5(PO4)3 + 4H2CO3 5Ca2+ + 3HPO42- + 4HCO3- + H2O Apatite (mineral) Bio-available P Weathering factors: Climate Parent material Topography Time Biota (Jenny 1941) Carbonic acid (CO2 from respiration e.g. plant roots)

21. Sources of P in soils: Mycorrhizal fungi  organic and inorganic P Brady & Weill (1999)

22. Sources of P in soils: (Phosphatase) enzymes  organic P Species A Species B Species C Species D Dissolved phosphate Monoester (labile org P) Diester Inosotol P (refractory) Hypothesis of increasing investment in organic P acquisition Turner (2008)

23. How important are P inputs relative to internal cycles? Chapin et al. (2002) – Table 8.1

24. P cycling in water Forms of P in water: DOP • Movement: • water • wind (dust) • animals PIP POP DIP uM P POP Total P (filter) PIP DOP TDP (Total dissolved P) DIP (PO43-) Key additional control: Redox related to element interactions D/P = dissolved/particulate I/O = inorganic/organic

25. Redox affects P via Fe: Internal eutrophication External P load ↑ production Mixing (without re-ppt) Sedimentation and decomposition ↑ anoxia ↑ sediment P and Fe2+ release Fe3+ reduction in absence of DO (or NO3-) Loss of sorption ability ↓ FeOOH with associated PO43- Bottom water chemistry Fe2+ DIP DO Classic studies: Mortimer, Einsele Current Netherlands focus: Smolders et al. (2006) review Time

26. As Fe increases in sediments, P may increase ... and may be released under reducing conditions. Fe/Al-P Smolders et al. (2006)

27. Sulfur can intensify internal eutrophication: SO42- HS- • Alkalinity  • Greater decay rate (acid neutralization) • HCO3- competes with PO43- for anion exchange sites ↑ HCO3- ●= sulfate addition (all in waterlogged conditions) ↑ NH4+ ↑ PO43-

28. Smolders et al. (2006)

29. P like N: • Internal cycling dominates P available for plant uptake P unlike N: • No P-focused oxidation-reduction reactions (redox controls are via interactions with other elements) • Using N to obtain P: Microbes (incl. mycorrhizae) & plants produce phosphatases to access organic P • No important gas phase • Main pools in soils/sediments Cycle essentially uni-directional

30. Questions to consider • Why phosphorus? • Phosphorus cycling • How does global cycle P differ from N? • Forms, pools, fluxes • P cycling in soils vs. inland waters vs. marine systems • Controls on availability & interactions with other elements • Why care about phosphorus inputs and losses?

31. Humans have modified the P cycle • Flows of P have tripled since 1960 (Milennium Ecosystem Assessment) • P mining expected to peak ~2030 (Cordell et al. 2009) Data from Smil (2000)

32. Greater accumulation of P in soils… World Cropland P Balance Manure Will long-term P-accumulation drive future exports to surface waters? Extra P Fert. Loss Animal Crop After Bennett et al. (2001)

33. Leads to greater streamwater P in agricultural and urban areas... Orthophosphate (mg/L) Total P (mg/L) Muhller & Spahr (2006): USGS National Water-Quality Assessment Program, Scientific Investigations Report 2006–5107 Mixed Ag Partial Urban Undevel

34. Why care about nutrient inputs to aquatic systems? • Eutrophication: “...anthropogenic nutrient loading to aquatic ecosystems (i.e., cultural eutrophication; Hasler 1947) from both point and nonpoint sources typically results in rapid increases in the rate of biological production and significant reductions in water column transparency and can create a wide range of undesirable water quality changes in freshwater and marine ecosystems.” (Smith et al. 2006)

35. Effects of eutrophication • Marine dinoflagellates: red tides (fish kills, neurotoxins in shellfish) • Freshwater cyanobacteria (neurotoxins, hepatotoxins) • Phytoplankton blooms • Hypoxia/anoxia • Toxicity to wildlife

36. Cause of eutrophication which nutrient(s)? C? N? P? Classic and ongoing scientific investigations…

37. P linked to eutrophication in L. Washington... Chl-a Nutrient diversion Total P Year ... but soap/detergent interests suggested that decreases in phytoplankton had caused the decrease in P. Edmondson (1970, 1991....)

38. Next step: Whole-lake fertilizations, Experimental Lakes Area • P consistently limited growth • C could be obtained from atmospheric inputs C + N P Chlorophyll Total P Schindler (1977)

39. Why not N limitation? • N fixation greater where TN is low rel. to TP • Cyanobacteria alleviated N limitation inlakes Total N Planktonic N fixation Total P TN:TP loading ratio (molar) Data from Howarth et al. (1988); Schindler (1977)

40. Why P limitation? P sediments rapidly out of water column • P sediments out: • with organic matter • as precipitates with CaCO3, Fe, Mn • Legacy effect of re-mobilization: • Anoxic conditions  release Fe-P • Elevated CO2  release Ca-P 0-2 m PERCENT 32P SEDIMENTS Levine et al. (1986) DAYS AFTER ADDITION

41. Schindler et al. (2008) • Fertilization • High N:P (12:1) • Low N:P (4:1) • III-V. no N fertilization • IV. Predatory fish (pike) present TP TDP TN TIN TN:TP TIN:TDP

42. Are estuaries and coastal zones N or P limited? • Yes: P mgmt is needed in estuaries: • evidence in some estuaries of N fixation, and of production in response to P; • need whole-ecosystem approach before making costly decisions No: N limitation in many estuaries • low N fixers at high salinities – likely b/c SO4 inhibits N-fixer growth • mixing of low N:P waters (from offshore, & b/c of high coastal denitrification) promotes N limitation • greater P availability in estuaries than lakes • nutrient loads often at low N:P, increasing N limitation

43. “...controlling the eutrophication of coastal zone waters will likely require careful basin-specific management practices for both N and P.” (Smith 2006) P limitation Redfield ratio (16:1 by moles) N limitation Smith (2006)

44. Redfield ratio: marine algae = water column = N:P 16:1 P limitation [NO3-] (μmol kg-1) N limitation Orig. by Redfield (1934) [PO43-] (μmol kg-1)

45. Marine nutrient limitation more variable • N:P ~16:1 (molar) = Redfield ratio • N:P < 16(-20): N limitation • N:P > 16: P limitation • N limitation typical in coastal zones (Howarth & Marino 2006) • (Terrestrial: N-limited in temperate zone; P-limited on older tropical soils) Chapin et al.(2002) – Fig. 10.7, from Valiela (1995)

46. Break (15 min)Discussion (Childers et al. 2011)and summary

47. P sustainability challenges: human food Pools and fluxes Key P flows • P mining • Agricultural P use • non agricultural P uses • P in food • A) P recycled in farm operations • B) P lost from farm fields • C) P lost in food processing • /transportation • A) P composted in food waste • B) P in human excreta • P lost to landfills • A) P from sewage P treatment recycled as fertilizer • B) P discharged in sewage treatment Childers (2011)

48. P sustainability challenges: human food • What is meant by “non-substitutability” of P resources? • What are the prospects for increasing P availability to agriculture? • What are benefits and obstacles of different strategies to close P cycle? • GMO pig to reduce P in animal waste?

49. Species identity and the P cycle • In what ways is species identity important to ecosystem functioning in • The terrestrial P cycle? • The aquatic P cycle? • The agricultural P cycle?

50. Summary of the P cycle • Soil/sediment-focused, ~unidirectional at human time scales • Limiting element in aquatic systems (particularly freshwater) and at long time scales • Complex interactions with other elements • Altered considerably by human activities (like all the cycles)