The pitcher plant Sarracenia purpurea can directly acquire organic nitrogen and short-circuit the inorganic nitrogen cycle

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Karagatzides, Jim D ^a   Butler, Jessica L ^a   Ellison, Aaron M ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMMONIUM NITRATE; GLYCINE; ORGANIC NITROGEN; PHENYLALANINE; NITROGEN;

AMINO ACID TRANSPORT; ARTICLE; CANADA; CARNIVOROUS PLANT; CONTROLLED STUDY; FOOD WEB; NITROGEN AVAILABILITY; NITROGEN CYCLE; NITROGEN DEPOSITION; NITROGEN MINERALIZATION; NITROGEN UPTAKE; NONHUMAN; PREDATOR PREY INTERACTION; SARRACENIA PURPUREA; UNITED STATES; METABOLISM; SARRACENIACEAE;

SARRACENIA PURPUREA; SARRACENIACEAE; TRACHEOPHYTA;

NITROGEN; SARRACENIACEAE;

EID: 67650243245     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006164     Document Type: Article

References (67)

1. Vitousek PM, Aber J, Howarth RW, Likens GE, Matson PA, et al. (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol App 7: 737-750.
2. Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75: 2373-2383.
3. Henry HAL, Jefferies RL (2002) Free amino acid, ammonium and nitrate concentrations in soil solutions of a grazed coastal marsh in relation to plant growth. Plant Cell Env 25: 665-675.
4. Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250: 283-292.
5. Persson J, Nasholm T (2001) Amino acid uptake: a widespread ability among boreal forest plants. Ecol Lett 4: 434-438.
6. Bridgham SD, Pastor J, Janssens JA, Chapin CT, Malterer TJ (1996) Multiple limiting gradients in peatlands: a call for a new paradigm. Wetlands 16: 45-65.
7. Senwo ZN, Tabatabai MA (1998) Amino acid composition of soil organic matter. Biol Fert Soil 26: 235-242.
8. Jones DL, Farrar JF, Newsham KK (2004) Rapid amino acid cycling in Arctic and Antarctic soils. Water Air Soil Pollut, Focus 4: 169-175.
9. McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, et al. (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415: 68-71.
10. Miller AE, Bowman WD, Nash Suding K (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88: 1832-1840.
11. Wiegelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142: 627-635.
12. Virtanen AI, Linkola H (1946) Organic nitrogen compounds as nitrogen nutrition for higher plants. Nature 158: 515.
13. Melin E, Nilsson H (1953) Transfer of labelled nitrogen from glutamic acid to pine seedlings through the mycelium of Boletus variegatus (Sw.) Fr. Nature 171: 134.
14. Miller RH, Schmidt EL (1965) Uptake and assimilation of amino acids supplied to the sterile soil: root environment of the bean plant ( Phaseolus vulgaris). Soil Sci 100: 323-330.
15. Lipson D, Nasholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128: 305-316.
16. Stark JM (2000) Nutrient transformations. In: Sala OE, Jackson RB, Mooney HA, Howarth RW, eds. Methods in ecosystem science. New York: Springer-Verlag. pp 215-234.
17. Neff JC, Chapin FS, Vitousek PM (2003) Breaks in the cycle: dissolved organic nitrogen in terrestrial ecosystems. Front Ecol Env 1: 205-211.
18. Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Ann Rev Plant Physiol 36: 77-115.
19. Ellison AM, Gotelli NJ (2001) Evolutionary ecology of carnivorous plants. Trends Ecol Evol 16: 623-629.
20. Givnish TJ (1989) Ecology and evolution of carnivorous plants. In: Abrahamson WG, ed. Plant-Animal Interactions. New York: McGraw-Hill. pp 242-290.
21. Porembski S, Barthlott W (2000) Inselbergs: biotic diversity of isolated rock outcrops in tropical and temperate regions. Berlin: Springer-Verlag. pp 524.
22. Butler JL, Ellison AM (2007) Nitrogen cycling dynamics in the carnivorous northern pitcher plant, Sarracenia purpurea. Func Ecol 21: 835-843.
23. Chapin CT, Pastor J (1995) Nutrient limitations in the northern pitcher plant Sarracenia purpurea. Can J Bot 73: 728-734.
24. Schulze W, Schulze E-D, Pate JS, Gillison AN (1997) The nitrogen supply from soils and insects during growth of the pitcher plants Nepenthes mirabilis, Cephalotus follicularis and Darlingtonia californica. Oecologia 112: 464-471.
25. Hepburn JS, Jones FM, St. John EQ (1927) The biochemistry of the American pitcher plants. Trans Wagner Free Inst Sci 11: 1-95.
26. Gallie DR, Chang SC (1997) Signal transduction in the carnivorous plant Sarracenia purpurea. Plant Physiol 115: 1461-1471.
27. Addicott JF (1974) Predation and prey community structure: an experimental study of the effect of mosquito larvae on the protozoan communities of pitcher plants. Ecology 55: 475-492.
28. Naeem S (1988) Resource heterogeneity fosters coexistence of a mite and a midge in pitcher plants. Ecol Mono 58: 215-227.
29. Bradshaw WE, Creelman RA (1984) Mutualism between the carnivorous purple pitcher plant Sarracenia purpurea and its inhabitants. Am Midl Nat 112: 294-304.
30. Butler JL, Gotelli NJ, Ellison AM (2008) Linking the brown and green: nutrient transformation and fate in the Sarracenia microecosystem. Ecology 89: 898-904.
31. Ellison AM, Gotelli NJ (2002) Nitrogen availability alters the expression of carnivory in the northern pitcher plant Sarracenia purpurea. Proc Natl Acad Sci U S A 99: 4409-4412.
32. Gotelli N J, Ellison AM (2002) Nitrogen deposition and extinction risk in the northern pitcher plant Sarracenia purpurea. Ecology 83: 2758-2765.
33. Bedford BL, Walbridge MR, Aldous A (1999) Patterns in nutrient availability and plant diversity of temperate North American wetlands. Ecology 80: 2151-2169.
34. Clemmensen KE, Sorensen PL, Michelsen A, Jonasson S, Ström L (2008) Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155: 771-738.
35. Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil processes. Ecology 80: 2408-2419.
36. Darwin C (1875) Insectivorous plants. New York: Appleton and Company. 462 p.
37. Ellison AM, Gotelli NJ (2009) Energetics and the evolution of carnivorous plants - Darwin's "most wonderful plants in the world". J Exp Bot 60: 19-42.
38. Lloyd FE (1942) The carnivorous plants. New York: Ronald Press. 352 p.
39. Gotelli NJ, Ellison AM (2006) Food-web models predict species abundance in response to habitat change. PLoS Biol 44: e324.
40. Peterson CN, Day S, Wolfe BE, Ellison AM, Kolter R, et al. (2008) A keystone predator controls bacterial diversity in the pitcher plant ( Sarracenia purpurea) microecosystem. Env Microbiol 10: 2257-2266.
41. Damman AWH (1990) Nutrient status of ombrotrophic peat bogs. Aquilo Ser Bot 28: 5-14.
42. Schnell DE (2002) Carnivorous plants of the United States and Canada, 2nd edition. Portland: Timber Press. 468 p.
43. Cochran-Stafira DL, von Ende CN (1998) Integrating bacteria into food webs: studies with Sarracenia purpurea inquilines. Ecology 79: 880-898.
44. Heard SB (1994) Pitcher plant midges and mosquitoes: a processing chain commensalism. Ecology 75: 1647-1660.
45. Newell SJ, Nastase, AJ (1998) Efficiency of insect capture by Sarracenia purpurea (Sarraceniaceae), the northern pitcher plant. Am J Bot 85: 88-91.
46. Błedzki LA, Ellison AM (1998) Population growth and production of Habrotrocha rosa Donner (Rotifera: Bdelloidea) and its contribution to the nutrient supply of its host, the northern pitcher plant, Sarracenia purpurea L. (Sarraceniaceae). Hydrobiologia 385: 193-200.
47. Błedzki LA, Ellison AM (2002) Nutrient regeneration by rotifers in New England (USA) bogs. Ver Int Ver Limnol 28: 1328-1331.
48. Environment Canada (2004) Canadian acid deposition science assessment. Toronto: Meteorological Service of Canada. 479 p.
49. Swan JM, Gill AM (1970) The origins, spread, and consolidation of a floating bog in Harvard Pond, Petersham, Massachusetts. Ecology 51: 829-840.
50. National Atmospheric Deposition Program (NRSP-3) (2009) Champaign, Illinois: NADP Program Office, Illinois State Water Survey.
51. Plummer GL, Kethley JB (1964) Foliar absorption of amino acids, peptides, and other nutrients by the pitcher plant, Sarracenia flava. Bot Gaz 125: 245-260.
52. Lüttge U (1965) Untersuchungen zur Physiologie der Carnivoren-Drusen. II. Mitteilung. Über die Resorption verschiedener Substanzen. Planta 66: 331-334.
53. Heard S (1998) Capture rates of invertebrate prey by the pitcher plant, Sarracenia purpurea L. Am Midl Nat 139: 79-89.
54. Persson J, Hogberg P, Ekblad A, Hogberg M, Nordgren A, et al. (2003) Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia 137: 252-257.
55. Nadelhoffer K, Fry B (1994) Nitrogen isotope studies in forested ecosystems. In: Michener RH, Lajtha K, eds. Methods in ecology: stable isotopes in ecology and environmental science. London: Blackwell Scientific Publications. pp 22-44.
56. Nasholm T, Ekblad A, Nordin A, Giesler R, Hogberg M, et al. (1998) Boreal forest plants take up organic nitrogen. Nature 392: 914-916.
57. Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88: 989-999.
58. von Felton S, Buchmann N, Scherer-Lorenzen M (2008) Preferences for different nitrogen forms by coexisting plant species and soil microbes: comment. Ecology 89: 878-879.
59. Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5: 304-307.
60. Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microbes for specific amino acids. Biol Fert Soil 29: 257-261.
61. Nordin A, Hogberg P, Nasholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129: 125-132.
62. Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361: 150-153.
63. Nordin A, Schmidt I, Shaver G (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85: 955-962.
64. Finzi AD, Berthrong ST (2005) The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology 86: 3345-3353.
65. Atkin OK (1996) Reassessing the nitrogen relations of Arctic plants: a mini review. Plant Cell Env 19: 695-704.
66. Ellison AM, Gotelli NJ, Brewer JS, Cochran-Stafira DL, Kneitel J, et al. (2003) The evolutionary ecology of carnivorous plants. Adv Ecol Res 33: 1-74.
67. Fish D, Hall DW (1978) Succession and stratification of aquatic insects inhabiting the leaves of the insectivorous pitcher plant Sarracenia purpurea. Am Midl Nat 99: 172-183.