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Biotic nitrogen fixation in the bryosphere is inhibited more by drought than warming

Abstract

The boreal forest is of particular interest to climate change research due to its large circumpolar distribution and accumulated soil carbon pool. Carbon uptake in this ecosystem is nitrogen (N)-limited, therefore factors affecting carbon or nitrogen dynamics in the boreal forest can have consequences for global climate. We used a 2-year field experiment to investigate the response of biotic nitrogen fixation by cyanobacteria associated with boreal forest bryophytes, in a factorial experiment combining simulated climate change with habitat fragmentation treatments. We simulated climate change conditions using open-top greenhouse chambers in the field, which increased mean and maximum temperatures, and created a precipitation gradient from ambient levels in the center to extreme drought conditions at the periphery of the chamber. The dry patches near the chamber walls exhibited almost no N-fixation, despite having similar densities of cyanobacteria (predominantly Stigonema sp.) as other patches. Rates of N-fixation were best explained by a model containing moisture, fragmentation, cyanobacteria density and time; warming was not a significant variable affecting N-fixation. There was no significant interaction between warming and fragmentation. These results suggest that cyanobacteria responded physiologically to drought by reducing N-fixation activity long before any changes in density. Ecosystem processes, such as N-fixation, can respond in the short term to environmental change much more rapidly than changes in the underlying community structure. Such rapid physiological responses may occur faster than demographic insurance effects of biodiversity.

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References

  1. Ahn CY, Park MH, Joung SH, Kim HS, Jang KY, Oh HM (2003) Growth inhibition of cyanobacteria by ultrasonic radiation: laboratory and enclosure studies. Environ Sci Technol 37(13):3031–3037. doi:10.1021/es034048z

    CAS  Article  PubMed  Google Scholar 

  2. Belnap J (2001) Factors influencing nitrogen fixation and nitrogen release in biological soil crusts. In: Baldwin IT, Caldwell MM, Heldmaier G, Mooney HA, Schulze ED, Sommer U, Belnap J, Lange OL, Lange OL (eds) Biological soil crusts: structure, function, and management, vol 150. Springer, Berlin, Heidelberg, pp 241–261

    Chapter  Google Scholar 

  3. Bewley JD (1995) Physiological aspects of desiccation tolerance—a retrospect. Int J Plant Sci 156(4):393–403. doi:10.2307/2475057

    Article  Google Scholar 

  4. Birkemoe T, Liengen T (2000) Does collembolan grazing influence nitrogen fixation by cyanobacteria in the high Arctic? Polar Biol 23(8):589–592. doi:10.1007/s003000000133

    Article  Google Scholar 

  5. Bonan GB, Van Cleve K (1992) Soil temperature nitrogen mineralization and carbon source-sink relationships in boreal forests. Can J For Res 22(5):629–639. doi:10.1139/x92-084

    CAS  Article  Google Scholar 

  6. Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES, Brander KM, Brown C, Bruno JF, Duarte CM, Halpern BS, Holding J, Kappel CV, Kiessling W, O’Connor MI, Pandolfi JM, Parmesan C, Schwing FB, Sydeman WJ, Richardson AJ (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science 334(6056):652–655. doi:10.1126/science.1210288

    CAS  Article  PubMed  Google Scholar 

  7. Calcagno V, de Mazancourt C (2010) glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34(12):1–29

    Article  Google Scholar 

  8. Chapin FS III, Oechel WC, Van Cleve K, Lawrence W (1987) The role of mosses in the phosphorus cycling of an Alaskan USA black spruce forest. Oecologia 74(2):310–315. doi:10.1007/BF00379375

    Article  Google Scholar 

  9. Cohen JL, Furtado JC, Barlow MA, Alexeev VA, Cherry JE (2012) Arctic warming, increasing snow cover and widespread boreal winter cooling. Environ Res Lett 7(1):014007. doi:10.1088/1748-9326/7/1/014007

  10. DeLuca T, Zackrisson O, Gentili F, Sellstedt A, Nilsson MC (2007) Ecosystem controls on nitrogen fixation in boreal feather moss communities. Oecologia 152(1):121–130. doi:10.1007/s00442-006-0626-6

    Article  PubMed  Google Scholar 

  11. DeLuca TH, Zackrisson O, Nilsson MC, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419(6910):917–920. doi:10.1038/nature01051

    CAS  Article  PubMed  Google Scholar 

  12. DeLuca TH, Zackrisson O, Gundale MJ, Nilsson MC (2008) Ecosystem feedbacks and nitrogen fixation in boreal forests. Science 320(5880):1181. doi:10.1126/science.1154836

  13. Elmendorf SC, Henry GHR, Hollister RD, Callaghan TV, Collier LS, Cooper EJ, Cornelissen JHC, Day TA, Fosaa AM, Gould WA, Grétarsdóttir J, Harte J, Hermanutz L, Hik DS, Hofgaard A, Jarrad F, Jónsdóttir IS, Keuper F, Klanderud K, Klein JA, Koh S, Kudo G, Lang SI, Loewen V, May JL, Mercado J, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Pieper S, Post E, Rixen C, Robinson CH, Schmidt NM, Shaver GR, Stenström A, Tolvanen A, Totland C, Troxler T, Wahren CH, Webber PJ, Welker JM, Wookey PA (2012) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol Lett 15(2):164–175. doi:10.1111/j.1461-0248.2011.01716.x

  14. Environment Canada (2012) Canadian climate normals or averages 1971–2000. Available at: http://climate.weatheroffice.gc.ca/climate_normals/index_e.html. Accessed 6 May 2012

  15. Fitzjarrald DR, Moore KE (1994) Growing-season boundary-layer climate and surface exchanges in a sub-arctic lichen woodland. J Geophys Res Atmos 99(D1):1899–1917. doi:10.1029/93jd01019

    Article  Google Scholar 

  16. Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8(15):1–27

    Article  Google Scholar 

  17. Gentili F, Nilsson MC, Zackrisson O, DeLuca TH, Sellstedt A (2005) Physiological and molecular diversity of feather moss associative N2-fixing cyanobacteria. J Exp Bot 56(422):3121–3127. doi:10.1093/jxb/eri309

    CAS  Article  PubMed  Google Scholar 

  18. Gonzalez A, Loreau M (2009) The causes and consequences of compensatory dynamics in ecological communities. Annu Rev Ecol Evol Syst 40(1):393–414. doi:10.1146/annurev.ecolsys.39.110707.173349

    Article  Google Scholar 

  19. Gonzalez A, Lawton JH, Gilbert FS, Blackburn TM, Evans-Freke I (1998) Metapopulation dynamics, abundance, and distribution in a microecosystem. Science 281(5385):2045–2047

    CAS  Article  PubMed  Google Scholar 

  20. Grant RF, Black TA, Gaumont-Guay D, Kljun N, Barr AG, Morgenstern K, Nesic Z (2006) Net ecosystem productivity of boreal aspen forests under drought and climate change: mathematical modelling with Ecosys. Agric For Meteorol 140(1–4):152–170. doi:10.1016/j.agrformet.2006.01.012

    Article  Google Scholar 

  21. Guillard RRL (2005) Purification methods for microalgae. In: Andersen RA (ed) Algal culturing techniques. Elsevier/Academic Press, Burlington

    Google Scholar 

  22. Gundale MJ, Gustafsson H, Nilsson MC (2009) The sensitivity of nitrogen fixation by a feathermoss-cyanobacteria association to litter and moisture variability in young and old boreal forests. Can J For Res 39(12):2542–2549. doi:10.1139/X09-160

    CAS  Article  Google Scholar 

  23. Gundale MJ, Nilsson M, Bansal S, Jäderlund A (2012) The interactive effects of temperature and light on biological nitrogen fixation in boreal forests. New Phytol 194(2):453–463. doi:10.1111/j.1469-8137.2012.04071.x

    CAS  Article  PubMed  Google Scholar 

  24. Gundale MJ, Wardle DA, Nilsson MC (2012) The effect of altered macroclimate on N-fixation by boreal feather mosses. Biol Lett 8(5):805–808. doi:10.1098/rsbl.2012.0429

    Article  PubMed  PubMed Central  Google Scholar 

  25. Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) Acetylene-ethylene assay for N2 fixation—laboratory and field evaluation. Plant Physiol 43(8):1185–1207

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Hawes I, Howard-Williams C, Vincent WF (1992) Desiccation and recovery of antarctic cyanobacterial mats. Polar Biol 12(6–7). doi:10.1007/BF00236981

  27. Heyder U, Schaphoff S, Gerten D, Lucht W (2011) Risk of severe climate change impact on the terrestrial biosphere. Environ Res Lett 6(3). doi:10.1088/1748-9326/6/3/034036

  28. Hollister RD, Webber PJ (2000) Biotic validation of small open-top chambers in a tundra ecosystem. Glob Chang Biol 6(7):835–842. doi:10.1046/j.1365-2486.2000.00363.x

    Article  Google Scholar 

  29. Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454(7202):327–U34. doi:10.1038/nature07028

    CAS  Article  PubMed  Google Scholar 

  30. Jackson BG, Martin P, Nilsson MC, Wardle DA (2010) Response of feather moss associated N2 fixation and litter decomposition to variations in simulated rainfall intensity and frequency. Oikos 120(4):570–581. doi:10.1111/j.1600-0706.2010.18641.x

    Article  Google Scholar 

  31. Lechowicz MJ, Adams MS (1978) Diurnal and seasonal structure of the climate at Scheffer Ville, Quebec. Arct Alp Res 10(1):95–104

    Article  Google Scholar 

  32. Lindahl BO, Taylor AFS, Finlay RD (2002) Defining nutritional constraints on carbon cycling in boreal forests: towards a less ’phytocentric’ perspective. Plant Soil 242(1):123–135. doi:10.1023/A:1019650226585

    CAS  Article  Google Scholar 

  33. Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolstrom M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manag 259(4):698–709. doi:10.1016/j.foreco.2009.09.023

    Article  Google Scholar 

  34. Lindo Z, Gonzalez A (2010) The bryosphere: an integral and influential component of the Earth’s biosphere. Ecosystems 13(4):612–627. doi:10.1007/s10021-010-9336-3

    Article  Google Scholar 

  35. Lindo Z, Whiteley JA (2011) Old trees contribute bio-available nitrogen through canopy bryophytes. Plant Soil 342(1–2):1–8. doi:10.1007/s11104-010-0678-6

    Google Scholar 

  36. Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci USA 100(22):12765–12770. doi:10.1073/pnas.2235465100

  37. Mäkipää R, Karjalainen T, Pussinen A, Kellomäki S (1999) Effects of climate change and nitrogen deposition on the carbon sequestration of a forest ecosystem in the boreal zone. Can J For Res 29(10):1490–1501. doi:10.1139/x99-123

    Article  Google Scholar 

  38. Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH, Levesque E, Molau U, Molgaard P, Parsons AN, Svoboda J, Virginia RA (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3(s1):20–32. doi:10.1111/j.1365-2486.1997.gcb136.x

    Article  Google Scholar 

  39. Markham JH (2009) Variation in moss-associated nitrogen fixation in boreal forest stands. Oecologia 161(2):353–359. doi:10.1007/S00442-009-1391-0

    Article  PubMed  Google Scholar 

  40. McNabb DH, Geist JM (1979) Acetylene-reduction assay of symbiotic N2 fixation under field conditions. Ecology 60(5):1070–1072. doi:10.2307/1936873

    CAS  Article  Google Scholar 

  41. Menge DNL, Hedin LO (2009) Nitrogen fixation in different biogeochemical niches along a 120,000-year chronosequence in New Zealand. Ecology 90(8):2190–2201. doi:10.1890/08-0877.1

    Article  PubMed  Google Scholar 

  42. Moore TR (1980) The nutrient status of subarctic woodland soils. Arct Alp Res 12(2):147–160

    CAS  Article  Google Scholar 

  43. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci USA 107:19368–19373. doi:10.1073/pnas.1006463107

  44. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100

    Article  Google Scholar 

  45. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42. doi:10.1038/nature01286

    CAS  Article  PubMed  Google Scholar 

  46. Payette S, Fortin MJ, Gamache I (2001) The subarctic forest-tundra: the structure of a biome in a changing climate. Bioscience 51(9):709–718. doi:10.1641/0006-3568(2001) 051[0709:TSFTTS]2.0.CO;2

    Article  Google Scholar 

  47. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org/

  48. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111(1):1–61

  49. Rousk K, Jones DL, DeLuca TH (2014) The resilience of nitrogen fixation in feather moss (Pleurozium schreberi)-cyanobacteria associations after a drying and rewetting cycle. Plant Soil 377(1–2):159–167. doi:10.1007/s11104-013-1984-6

    CAS  Article  Google Scholar 

  50. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287(5459):1770–1774. doi:10.1126/science.287.5459.1770

    CAS  Article  PubMed  Google Scholar 

  51. Sanderson MG, Hemming DL, Betts RA (2011) Regional temperature and precipitation changes under high-end (\(\ge\)4 degrees C) global warming. Philos Trans R Soc A Math Phys Eng Sci 369(1934):85–98. doi:10.1098/rsta.2010.0283

    CAS  Article  Google Scholar 

  52. Scherer S, Potts M (1989) Novel water stress protein from a desiccation-tolerant cyanobacterium. Purification and partial characterization. J Biol Chem 264(21):12546–12553

  53. Schöllhorn R, Burris RH (1967) Acetylene as a competitive inhibitor of N2 fixation. Proc Natl Acad Sci USA 58(1):213–216. doi:10.1073/pnas.58.1.213

    Article  PubMed  PubMed Central  Google Scholar 

  54. Shen KP, Harte J (2000) Ecosystem climate manipulations. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 353–369

    Chapter  Google Scholar 

  55. Soil Classification Working Group, Agriculture and Agri-Food Canada (1998) The Canadian system of soil classification, 3rd edn. Agriculture and Agri-Food Canada vol 41647. NRC Research Press, Ottawa. Available at: http://sis.agr.gc.ca/cansis/publications/manuals/1998-cssc-ed3/cssc3_manual

  56. Sokal RR, Rohlf FJ (1981) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Company, New York

    Google Scholar 

  57. Sorensen PL, Michelsen A (2011) Long-term warming and litter addition affects nitrogen fixation in a subarctic heath. Glob Chang Biol 17(1):528–537. doi:10.1111/j.1365-2486.2010.02234.x

    Article  Google Scholar 

  58. Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13(5):543–552. doi:10.1111/J.1461-0248.2010.01450.X

    Article  PubMed  Google Scholar 

  59. Taggart RE, Cross AT (2009) Global greenhouse to icehouse and back again: the origin and future of the boreal forest biome. Glob Planet Chang 65(3–4):115–121. doi:10.1016/j.gloplacha.2008.10.014

    Article  Google Scholar 

  60. Therneau TM, Atkinson B, Ripley B (2010) rpart: recursive partitioning, R package version 3.1-48. Available at: http://CRAN.R-project.org/package=rpart

  61. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427(6970):145–148. doi:10.1038/nature02121

    CAS  Article  PubMed  Google Scholar 

  62. Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106(3):395–409. doi:10.1639/05

    Article  Google Scholar 

  63. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(1):1–45. doi:10.1023/A:1015798428743

    Article  Google Scholar 

  64. Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jonsdottir IS, Klein JA, Magnusson B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland O, Turner PL, Tweedie CE, Webber PJ, Wookey PA (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103(5):1342–1346

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Watkinson AR, Gill JA (2002) Climate change and dispersal. In: Bullock JM, Kenward RE, Hails RS (eds) Dispersal ecology. Blackwell Science, Malden, pp 410–428

    Google Scholar 

  66. Whiteley J (2012) Climate change and habitat fragmentation in a boreal forest bryosphere experiment. PhD thesis. McGill University, Montreal

  67. Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21(12):1–20

  68. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York. doi:10.1007/978-0-387-98141-3

  69. Wickham H (2011) plyr: tools for splitting, applying and combining data, R package version 1.4. Available at: http://CRAN.R-project.org/package=plyr

  70. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96(4):1463–1468. doi:10.1073/pnas.96.4.1463

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. Zackrisson O, DeLuca TH, Nilsson MC, Sellstedt A, Berglund LM (2004) Nitrogen fixation increases with successional age in boreal forests. Ecology 85(12):3327–3334. doi:10.1890/04-0461

    Article  Google Scholar 

  72. Zackrisson O, DeLuca T, Gentili F, Sellstedt A, Jäderlund A (2009) Nitrogen fixation in mixed Hylocomium splendens moss communities. Oecologia 160(2):309–319. doi:10.1007/s00442-009-1299-8

  73. Zehr JP, Montoya J (2007) Measuring N2 fixation in the field. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Boston, pp 193–205

    Chapter  Google Scholar 

  74. Zhang G, Zhang P, Liu H, Wang B (2006) Ultrasonic damages on cyanobacterial photosynthesis. Ultrason Sonochem 13(6):501–505. doi:10.1016/j.ultsonch.2005.11.001

    CAS  Article  PubMed  Google Scholar 

  75. Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Statistics for Biology and Health. Springer, New York. Available at: http://www.highstat.com/book1.htm

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Acknowledgments

This project was supported by a Post-Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada (NSERC) to JAW, with a Natural Sciences and Engineering Research Council discovery grant and Canada Research Chair funding to AG. Z. Lindo helped with field work and provided friendly review during manuscript preparation. O. Choulik provided logistical support, and many nourishing meals, in Schefferville. M. Mehta helped with cyanobacteria data collection. J. Connolly provided helpful advice on mixed modeling approaches. The manuscript was greatly improved by constructive comments from three reviewers.

Author contribution statement

JAW and AG conceived and designed the experiment. JAW conducted fieldwork, collected and processed samples, and analyzed the data; JAW and AG analyzed the temperature data. JAW wrote the manuscript, AG provided editorial advice.

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Correspondence to Jonathan A. Whiteley.

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Communicated by Amy Austin.

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Whiteley, J.A., Gonzalez, A. Biotic nitrogen fixation in the bryosphere is inhibited more by drought than warming. Oecologia 181, 1243–1258 (2016). https://doi.org/10.1007/s00442-016-3601-x

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Keywords

  • Climate-change
  • Habitat fragmentation
  • Nitrogen fixation
  • Cyanobacteria
  • Pleurozium schreberi
  • Boreal forest