Ecosystems

, Volume 14, Issue 7, pp 1066–1080

Responses of Ecosystem Carbon Cycling to Climate Change Treatments Along an Elevation Gradient

  • Zhuoting Wu
  • George W. Koch
  • Paul Dijkstra
  • Matthew A. Bowker
  • Bruce A. Hungate
Article

Abstract

Global temperature increases and precipitation changes are both expected to alter ecosystem carbon (C) cycling. We tested responses of ecosystem C cycling to simulated climate change using field manipulations of temperature and precipitation across a range of grass-dominated ecosystems along an elevation gradient in northern Arizona. In 2002, we transplanted intact plant–soil mesocosms to simulate warming and used passive interceptors and collectors to manipulate precipitation. We measured daytime ecosystem respiration (ER) and net ecosystem C exchange throughout the growing season in 2008 and 2009. Warming generally stimulated ER and photosynthesis, but had variable effects on daytime net C exchange. Increased precipitation stimulated ecosystem C cycling only in the driest ecosystem at the lowest elevation, whereas decreased precipitation showed no effects on ecosystem C cycling across all ecosystems. No significant interaction between temperature and precipitation treatments was observed. Structural equation modeling revealed that in the wetter-than-average year of 2008, changes in ecosystem C cycling were more strongly affected by warming-induced reduction in soil moisture than by altered precipitation. In contrast, during the drier year of 2009, warming induced increase in soil temperature rather than changes in soil moisture determined ecosystem C cycling. Our findings suggest that warming exerted the strongest influence on ecosystem C cycling in both years, by modulating soil moisture in the wet year and soil temperature in the dry year.

Key words

warming precipitation gross ecosystem photosynthesis ecosystem respiration net ecosystem exchange structural equation model 

Supplementary material

10021_2011_9464_MOESM1_ESM.docx (2.3 mb)
Supplementary material 1 (DOCX 2318 kb)

References

  1. Adair K, Schwartz E. 2008. Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of Northern Arizona, USA. Microb Ecol 56:420–6.PubMedCrossRefGoogle Scholar
  2. Allison SD, Treseder KK. 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Change Biol 14:2898–909.CrossRefGoogle Scholar
  3. Antoninka A, Wolf JE, Bowker M, Classen AT, Johnson NC. 2009. Linking above- and belowground responses to global change at community and ecosystem scales. Glob Change Biol 15:914–29.CrossRefGoogle Scholar
  4. Atkin OK, Millar AH, Gardeström P, Day DA. 2000. Photosynthesis, carbohydrate metabolism, and respiration in leaves of higher plants. In: Legood RC, Sharkey TD, von Cammerer S, Eds. Photosynthesis: physiology and metabolism. Dordrecht: Kluwer Academic Publishers. p 153–75.Google Scholar
  5. Bellamy PH, Loveland PJ, Bradley RI, Lark RM, Kirk GJD. 2005. Carbon losses from all soils across England and Wales 1978–2003. Nature 437:245–8.PubMedCrossRefGoogle Scholar
  6. Blankinship JC, Brown JR, Dijkstra P, Allwright MC, Hungate BA. 2010. Responses of terrestrial CH4 uptake to interactive changes in precipitation and temperature along a climatic gradient. Ecosystem 13:1157–70.CrossRefGoogle Scholar
  7. Bontti EE, Decant JP, Munson SM, Gathany MA, Prezeszlowska A, Haddix ML, Owens S, Burke IC, Parton WJ, Harmon ME. 2009. Litter decomposition in grasslands of Central North America (US Great Plains). Glob Change Biol 15:1356–63.CrossRefGoogle Scholar
  8. Browne MW, Cudeck R. 1993. Alternative ways of assessing model fit. In: Bollen KA, Long JS, Eds. Testing structural equation models. Newbury Park, CA: Sage Publications. p 136–62.Google Scholar
  9. Chaudhary VB, Bowker MA, O’Dell TE, Grace JB, Redman AE, Rillig MC, Johnson NC. 2009. Untangling the biological contributions to soil stability in semiarid shrublands. Ecol Appl 19:110–22.PubMedCrossRefGoogle Scholar
  10. Chen S, Lin G, Huang J, He M. 2008. Responses of soil respiration to simulated precipitation pulses in semiarid steppe under different grazing regimes. J Plant Ecol 1:237–46.CrossRefGoogle Scholar
  11. Chen S, Lin G, Huang J, Jenerette GD. 2009. Dependence of carbon sequestration on the differential responses of ecosystem photosynthesis and respiration to rain pulses in a semiarid steppe. Glob Change Biol 15:2450–61.CrossRefGoogle Scholar
  12. Chimner RA, Welker JM, Morgan J, LeCain D, Reeder J. 2010. Experimental manipulations of winter snow and summer rain influence ecosystem carbon cycling in a mixed-grass prairie, Wyoming, USA. Ecohydrology 3:284–93.CrossRefGoogle Scholar
  13. Chou WW, Silver WL, Jackson RD, Thompson AW, Allen-Diaz B. 2008. The sensitivity of annual grassland carbon cycling to the quantity and timing of rainfall. Glob Change Biol 14:1382–94.CrossRefGoogle Scholar
  14. Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon WT, Laprise R, Magana Rueda V, Mearns L, Menendez CG, Raisanen J, Rinke A, Sarr A, Whetton P. 2007. Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, Eds. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK/New York, NY: Cambridge University Press.Google Scholar
  15. Churkina G, Running SW, Schloss AL, Intercomparison TPOFTPNM. 1999. Comparing global models of terrestrial net primary productivity (NPP): the importance of water availability. Glob Change Biol 5:46–55.CrossRefGoogle Scholar
  16. Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ. 2000. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–7.PubMedCrossRefGoogle Scholar
  17. De Boeck HJ, Lemmens CM, Catherine MHM, Vicca S, Van den Berge J, Van Dongen S, Janssens IA, Ceulemans R, Nijs I. 2007. How do climate warming and species richness affect CO2 fluxes in experimental grasslands? New Phytol 175:512–22.PubMedCrossRefGoogle Scholar
  18. De Valpine P, Harte J. 2001. Plant responses to experimental warming in a montane meadow. Ecology 82:637–48.CrossRefGoogle Scholar
  19. Deng X, Joly RJ, Hahn T. 1990. The influence of water deficit on photosynthesis and translocation of 14C-labeled assimilates in cacao seedlings. Physiol Plant 78:623–7.CrossRefGoogle Scholar
  20. Dijkstra P, Ishizu A, Doucett R, Hart SC, Schwartz E, Menyailo OV, Hungate BA. 2006. 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257–66.CrossRefGoogle Scholar
  21. Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA. 2008. 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:389–97.PubMedCrossRefGoogle Scholar
  22. Dugas WA, Heuer ML, Mayeux HS. 1999. Carbon dioxide fluxes over bermudagrass, native prairie, and sorghum. Agric For Meteorol 93:121–39.CrossRefGoogle Scholar
  23. Dukes JS, Chiariello NR, Cleland EE, Moore LA, Shaw MR, Thayer S, Tobeck T, Mooney HA, Field CB. 2005. Responses of grassland production to single and multiple global environmental changes. PLoS Biol 3:1829–37.CrossRefGoogle Scholar
  24. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO. 2000. Climate extremes: observations, modeling, and impacts. Science 289:2068–74.PubMedCrossRefGoogle Scholar
  25. Emmett BA, Beier C, Estiarte M, Tietema A, Kristensen HL, Williams D, Peñuelas J, Schmidt I, Sowerby A. 2004. The response of soil processes to climate change: results from manipulation studies of shrublands across an environmental gradient. Ecosystems 7:625–37.CrossRefGoogle Scholar
  26. Frank AB, Dugas WA. 2001. Carbon dioxide fluxes over a northern, semiarid, mixed-grass prairie. Agric For Meteorol 108:317–26.CrossRefGoogle Scholar
  27. Garbulsky MF, Peñuelas J, Papale D, Ardo J, Goulden ML, Kiely G, Richardson AD, Rotenberg E, Veenendaal EM, Filella I. 2010. Patterns and controls of the variability of radiation use efficiency and primary productivity across terrestrial ecosystems. Glob Ecol Biogeogr 19:253–67.CrossRefGoogle Scholar
  28. Gorissen A, Tietema A, Joosten NN, Estiarte M, Peñuelas J, Sowerby A, Emmett BA, Beier C. 2004. Climate change affects carbon allocation to the soil in shrublands. Ecosystems 7:650–61.CrossRefGoogle Scholar
  29. Grace JB. 2006. Structural equation modeling and natural systems. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  30. Grace JB, Anderson TM, Smith MD, Seabloom E, Andelman SJ, Meche G, Weiher E, Allain LK, Julita H, Sankaran M, Knops J, Ritchie M, Willig MR. 2007. Does species diversity limit productivity in natural grassland communities? Ecol Lett 10:680–9.PubMedCrossRefGoogle Scholar
  31. Grime JP, Fridley JD, Askew AP, Thompson K, Hodgson JG, Bennett CR. 2008. Long-term resistance to simulated climate change in an infertile grassland. Proc Natl Acad Sci USA 105:10028–32.PubMedCrossRefGoogle Scholar
  32. Grogan P, Chapin FSIII. 2000. Initial effects of experimental warming on above- and belowground components of net ecosystem CO2 exchange in arctic tundra. Oecologia 125:512–20.CrossRefGoogle Scholar
  33. Harper CW, Blair JM, Fay PA, Knapp AK, Carlisle JD. 2005. Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem. Glob Change Biol 11:322–34.CrossRefGoogle Scholar
  34. Hartley AE, Neill C, Melillo JM, Crabtree R, Bowles FP. 1999. Plant performance and soil nitrogen mineralization in response to simulated climate change in subarctic dwarf shrub heath. Oikos 86:331–43.CrossRefGoogle Scholar
  35. Hobbie SE. 1996. Temperature plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–22.CrossRefGoogle Scholar
  36. Huxman T, Snyder K, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S. 2004. Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–68.PubMedGoogle Scholar
  37. Intergovernmental Panel on Climate Change (IPCC). 2007. Climate change 2007: the physical science basis-summary for policy makers. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC WGI 4th Assessment Report.Google Scholar
  38. Jónsdóttir IS, Khitun O, Stenström A. 2005. Biomass and nutrient responses of a clonal tundra sedge to climate warming. Can J Bot 83:1608–21.CrossRefGoogle Scholar
  39. Kirschbaum MUF. 1995. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol Biochem 27:753–60.CrossRefGoogle Scholar
  40. Knapp AK, Smith MD. 2001. Variation among biomes in temporal dynamics of aboveground primary production. Science 291:481–4.PubMedCrossRefGoogle Scholar
  41. Knapp AK, Beier C, Briske DD, Classen AT, Luo Y, Reichstein M, Smith MD, Smith SD, Bell JE, Fay PA, Heisler JL, Leavitt SW, Sherry R, Smith B, Weng E. 2008. Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58:811–21.CrossRefGoogle Scholar
  42. Laughlin DC, Hart SC, Kaye JP, Moore MM. 2010. Evidence for indirect effects of plant diversity and composition on net nitrification. Plant Soil 330:435–45.CrossRefGoogle Scholar
  43. Lawton D, Leahy P, Kiely G, Byrne KA, Calanca P. 2006. Modeling of net ecosystem exchange and its components for a humid grassland ecosystem. J Geophys Res 111:G04013. doi:10.1029/2006JG000160.CrossRefGoogle Scholar
  44. Lellei-Kovács E, Kovács-Láng E, Kalapos T, Botta-Dukát Z, Barabás S, Beier C. 2008. Experimental warming does not enhance soil respiration in a semiarid temperate forest-steppe ecosystem. Community Ecol 9:29–37.CrossRefGoogle Scholar
  45. Lieth H. 1973. Primary production: terrestrial ecosystems. Hum Ecol 1:303–32.CrossRefGoogle Scholar
  46. Lilley J, Bolger T, Gifford R. 2001. Productivity of Trifolium subterraneum and Phalaris aquatica under warmer, high CO2 conditions. New Phytol 150:371–83.CrossRefGoogle Scholar
  47. Liu W, Zhang Z, Wan S. 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob Change Biol 15:184–95.CrossRefGoogle Scholar
  48. Luo YQ, Gerten D, Le Maire G, Parton WJ, Weng ES, Zhou XH, Keogh C, Beier C, Ciais P, Cramer W, Dukes JS, Emmett B, Hanson PJ, Knapp A, Linder S, Nepstad D, Rustad L. 2008. Modeled interactive effects of precipitation, temperature, and [CO2] on ecosystem carbon and water dynamics in different climatic zones. Glob Change Biol 14:1986–99.CrossRefGoogle Scholar
  49. Luo Y, Sherry R, Zhou X, Wan S. 2009. Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest. GCB Bioenergy 1:62–74.CrossRefGoogle Scholar
  50. McHale PJ, Mitchell MJ, Bowles FP. 1998. Soil warming in a northern hardwood forest: trace gas fluxes and leaf litter decomposition. Can J For Res 28:1365–72.CrossRefGoogle Scholar
  51. Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173–6.PubMedCrossRefGoogle Scholar
  52. Menzel A, Fabian P. 1999. Growing season extended in Europe. Nature 397:659.CrossRefGoogle Scholar
  53. Mertens S, Nijs I, Heuer M, Kockelbergh F, Beyens L, Kerckvoorde Av, Impens I. 2001. Influence of high temperature on end-of-season tundra CO2 exchange. Ecosystems 4:226–36.CrossRefGoogle Scholar
  54. Mirzaei H, Kreyling J, Hussain MZ, Li Y, Tenhunen J, Beierkuhnlein C, Jentsch A. 2008. A single drought event of 100-year recurrence enhances subsequent carbon uptake and changes carbon allocation in experimental grassland communities. J Plant Nutr Soil Sci 171:681–9.CrossRefGoogle Scholar
  55. Neff JC, Hooper DU. 2002. Vegetation and climate controls on potential CO2, DOC and DON production in northern latitude soils. Glob Change Biol 8:872–84.CrossRefGoogle Scholar
  56. Niinistö SM, Silvola J, Kellomäki S. 2004. Soil CO2 efflux in a boreal pine forest under atmospheric CO2 enrichment and air warming. Glob Change Biol 10:1363–76.CrossRefGoogle Scholar
  57. Niu S, Wu M, Han Y, Xia J, Li L, Wan S. 2008a. Water-mediated responses of ecosystem carbon fluxes to climatic change in a temperate steppe. New Phytol 177:209–19.PubMedGoogle Scholar
  58. Niu S, Li Z, Xia J, Han Y, Wu M, Wan S. 2008b. Climatic warming changes plant photosynthesis and its temperature dependence in a temperate steppe of northern China. Environ Exp Bot 63:91–101.CrossRefGoogle Scholar
  59. Novick KA, Stoy PC, Katul GG, Ellsworth DS, Siqueira MBS, Juang J, Oren R. 2004. Carbon dioxide and water vapor exchange in a warm temperate grassland. Oecologia 138:259–74.PubMedCrossRefGoogle Scholar
  60. Oberbauer SF, Tweedie CE, Welker JM, Fahnestock JT, Henry GHR, Webber PJ, Hollister RD, Walker MD, Kuchy A, Elmore E, Starr G. 2007. Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecol Monogr 77:221–38.CrossRefGoogle Scholar
  61. Potts DL, Huxman TE, Scott RL, Williams DG, Goodrich DC. 2006. The sensitivity of ecosystem carbon exchange to seasonal precipitation and woody plant encroachment. Oecologia 150:453–63.PubMedCrossRefGoogle Scholar
  62. Pugesek B, Tomer A, Von Eye A. 2003. Structural equation modeling: applications in ecological and evolutionary biology. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  63. Risch AC, Frank DA. 2006. Carbon dioxide fluxes in a spatially and temporally heterogeneous temperate grassland. Oecologia 147:291–302.PubMedCrossRefGoogle Scholar
  64. Risch AC, Frank DA. 2007. Effects of increased soil water availability on grassland ecosystem carbon dioxide fluxes. Biogeochemistry 86:91–103.CrossRefGoogle Scholar
  65. Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JH, Gurevitch J. 2001. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–62.CrossRefGoogle Scholar
  66. Saleska SR, Miller SD, Matross DM, Goulden ML, Wofsy SC, da Rocha HR, de Camargo PB, Crill P, Daube BC, de Freitas HC, Hutyra L, Keller M, Kirchhoff V, Menton M, Munger JW, Pyle EH, Rice AH, Silva H. 2003. Carbon in Amazon forests: unexpected seasonal fluxes and disturbance-induced losses. Science 302:1554–7.PubMedCrossRefGoogle Scholar
  67. Sardans J, Penuuelas J, Estiarte M, Prieto P. 2008. Warming and drought alter C and N concentration, allocation and accumulation in a Mediterranean shrubland. Glob Change Biol 14:2304–16.CrossRefGoogle Scholar
  68. Schindlbacher A, Zechmeister-Boltenstern S, Jandl R. 2009. Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob Change Biol 15:901–13.CrossRefGoogle Scholar
  69. Schipper LA, Baisden WT, Parfitt RL, Ross C, Claydon JJ, Arnold G. 2007. Large losses of soil C and N from soil profiles under pasture in New Zealand during the past 20 years. Glob Change Biol 13:1138–44.CrossRefGoogle Scholar
  70. Schwartz E, Blazewicz S, Doucett R, Hungate BA, Hart SC, Dijkstra P. 2007. Natural abundance δ15N and δ13C of DNA extracted from soil. Soil Biol Biochem 39:3101–7.CrossRefGoogle Scholar
  71. Scott RL, Hamerlynck EP, Jenerette GD, Moran MS, Barron-Gafford GA. 2010. Carbon dioxide exchange in a semidesert grassland through drought-induced vegetation change. J Geophys Res Biogeosci 115:G03026. doi:10.1029/2010JG001348.CrossRefGoogle Scholar
  72. Scurlock JMO, Johnson K, Olson RJ. 2002. Estimating net primary productivity from grassland biomass dynamics measurements. Glob Change Biol 8:736–53.CrossRefGoogle Scholar
  73. Seager R, Vecchi GA. 2010. Greenhouse warming and the 21st century hydroclimate of southwestern North America. Proc Natl Acad Sci USA 107:21277–82.PubMedCrossRefGoogle Scholar
  74. Seager R, Ting MF, Held I, Kushnir Y, Lu J, Vecchi G, Huang HP, Harnik N, Leetmaa A, Lau NC, Li CH, Velez J, Naik N. 2007. Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316:1181–4.PubMedCrossRefGoogle Scholar
  75. Shaver G, Canadell J, Chapin FSIII, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L. 2000. Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50:871–82.CrossRefGoogle Scholar
  76. Sherry RA, Weng E, Arnone JAIII, Johnson DW, Schimel DS, Verburg PS, Wallace LL, Luo Y. 2008. Lagged effects of experimental warming and doubled precipitation on annual and seasonal aboveground biomass production in a tallgrass prairie. Glob Change Biol 14:2923–36.CrossRefGoogle Scholar
  77. Silver WL, Jackson RD, Allen-Diaz B. 2005. Soil carbon dynamics of California grasslands under altered soil moisture regimes. Kearney Foundation of Soil Science Final Report: 1–14.Google Scholar
  78. Soussana JF, Allard V, Pilegaard K, Ambus P, Ammann C, Campbell C, Ceschia E, Clifton-Brown J, Czobel S, Domingues R, Flechard C, Fuhrer J, Hensen A, Horvath L, Jones M, Kasper G, Martin C, Nagy Z, Neftel A, Raschi A, Baronti S, Rees RM, Skiba U, Stefani P, Manca G, Sutton M, Tuba Z, Valentini R. 2007. Full accounting of the greenhouse gas (CO2, N2O, CH4) budget of nine European grassland sites. Agric Ecosyst Environ 121:121–34.CrossRefGoogle Scholar
  79. Sullivan PF, Arens SJT, Chimner RA, Welker JM. 2008. Temperature and microtopography interact to control carbon cycling in a high arctic fen. Ecosystems 11:61–76.CrossRefGoogle Scholar
  80. Suyker AE, Verma SB, Burba GG. 2003. Interannual variability in net CO2 exchange of a native tallgrass prairie. Glob Change Biol 9:255–65.CrossRefGoogle Scholar
  81. Weiher E, Forbes S, Schauwecker T, Grace JB. 2004. Multivariate control of plant species richness and biomass in blackland prairie. Oikos 106:151–7.CrossRefGoogle Scholar
  82. Weltzin JF, Loik ME, Schwinning S, Williams D, Fay P, Haddad B, Harte J, Huxman T, Knapp A, Lin G, Pockman W, Shaw R, Small E, Smith M, Smith SD, Tissue D, Zak J. 2003. Assessing the response of terrestrial ecosystems to potential changes in precipitation. Bioscience 53:941–52.CrossRefGoogle Scholar
  83. Wu Z, Dijkstra P, Koch GW, Penuelas J, Hungate BA. 2010. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Change Biol. doi:10.1111/j.1365-2486.2010.02302.x.
  84. Xu L, Baldocchi DD. 2004. Seasonal variation in carbon dioxide exchange over a Mediterranean annual grassland in California. Agric For Meteorol 123:79–96.CrossRefGoogle Scholar
  85. Zavaleta ES, Shaw MR, Chiariello NR, Thomas BD, Cleland EE, Field CB, Mooney HA. 2003. Grassland responses to three years of elevated temperature, CO2, precipitation, and N deposition. Ecol Monogr 73:585–604.CrossRefGoogle Scholar
  86. Zhou X, Sherry RA, An Y, Wallace LL, Luo Y. 2006. Main and interactive effects of warming, clipping, and doubled precipitation on soil CO2 efflux in a grassland ecosystem. Glob Biogeochem Cycles 20:GB1003. doi:10.1029/2005GB002526.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Zhuoting Wu
    • 1
  • George W. Koch
    • 1
  • Paul Dijkstra
    • 1
  • Matthew A. Bowker
    • 2
  • Bruce A. Hungate
    • 1
  1. 1.Department of Biological Sciences and Merriam-Powell Center for Environmental ResearchNorthern Arizona UniversityFlagstaffUSA
  2. 2.US Geological Survey, Southwest Biological Science CenterNorthern Arizona UniversityFlagstaffUSA

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