Plant and Soil

, Volume 165, Issue 1, pp 55–65 | Cite as

Responses of soil biota to elevated atmospheric carbon dioxide

  • Elizabeth G. O'Neill
Soil Biota

Abstract

Increasing concentrations of atmospheric CO2 could have dramatic effects upon terrestrial ecosystems including changes in ecosystem structure, nutrient cycling rates, net primary production, C source-sink relationships and successional patterns. All of these potential changes will be constrained to some degree by below ground processes and mediated by responses of soil biota to indirect effects of CO2 enrichment. A review of our current state of knowledge regarding responses of soil biota is presented, covering responses of mycorrhizae, N-fixing bacteria and actinomycetes, soil microbiota, plant pathogens, and soil fauna. Emphasis will be placed on consequences to biota of increasing C input through the rhizosphere and resulting feedbacks to above ground systems. Rising CO2 may also result in altered nutrient concentrations of plant litter, potentially changing decomposition rates through indirect effects upon decomposer communities. Thus, this review will also cover current information on decomposition of litter produced at elevated CO2.

Summary

Predictably, the responses of soil biota to CO2 enrichment and the degree of experimental emphasis on them increase with proximity to, and intimacy with, roots. Symbiotic associations are all stimulated to some degree. Total plant mycorrhization increases with elevated CO2. VAM fungi increase proportionately with fine root length/mass increase. ECM fungi, however, exhibit greater colonization per unit root length/mass at elevated CO2 than at current atmospheric levels. Total N-fixation per plant increases in all species examined, although the mechanisms of increase, as well as the eventual benefit to the host relative to N uptake may vary. Microbial responses are unclear. The assumption that changes in root exudation will drive increased mineralization and facilitate nutrient uptake should be examined experimentally, in light of recent models. Microbial results to date suggest that metabolic activity (measured as changes in process rates) is stimulated by root C input, rather than population size (measured by cell or colony counts). Insufficient evidence exists to predict responses of either soil-borne plant pathogens or soil fauna (i.e., food web responses). These are areas requiring attention, the first for its potential to limit ecosystem production through disease and the second because of its importance to nutrient cycling processes. Preliminary data on foliar litter decomposition suggests that neither nutrient ratios nor decomposition rates will be affected by rising CO2. This is another important area that may be better understood as the number of longer term studies with more realistic CO2 exposures increase. Evidence continues to mount that C fixation increases with CO2 enrichment and that the bulk of this C enters the belowground component of ecosystems. The global fate and effects of this additional C may affect all hierarchical levels, from organisms to ecosystems, and will be largely determined by responses of soil biota.

Key words

CO2 enrichment decomposition mycorrhizae nitrogen fixation rhizosphere soil biota soil fauna 

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References

  1. Ågren G I, McMurtie R E, Parton W J, Pastor J and Shugart H H 1991 State-of-the-art of models of production-decomposition linkages in conifer and grassland ecosystems. Ecol. Appl. 1, 118–138.Google Scholar
  2. Azcón R, Barea J M and Hayman D S 1976 Utilization of rock phosphate in alkaline soils by plants inoculated with mycorrhizal fungi and phosphate-solubilizing bacteria. Soil Biol. Biochem. 8, 135–138.CrossRefGoogle Scholar
  3. Allen M F 1987 Ecology of vesicular-arbuscular mycorrhizae in an arid ecosystem: use of natural processes promoting dispersal and establishment. In Mycorrhizae in the Next Decade: Practical Implications and Research Priorities. Eds. D MSylvia, L LHung and J HGraham pp 133–135. University of Florida, Gainesville, Florida.Google Scholar
  4. Allen M F 1991 The Ecology of Mycorrhizae. Cambridge University Press, New York. 184 p.Google Scholar
  5. Allen M F, Hipps L E and Woolridge G L 1989 Wind dispersal and subsequent establishment of VA mycorrhizal fungi across a successional landscape. Landscape Ecol. 2, 165–167CrossRefGoogle Scholar
  6. Arnone J AIII and Gordon J C 1990 Effect of nodulation, nitrogen fixation and CO2 enrichment on physiology, growth and dry mass allocation of seedlings of Alnus rubra Bong. New Phytol. 116, 55–66.CrossRefGoogle Scholar
  7. Blair J M, Parmalee R W and Beare M H 1990 Decay rates, nitrogen fluxes and decomposer communities of single- and mixed-species foliar litter. Ecology 71, 1976–1985.CrossRefGoogle Scholar
  8. Bledsoe C S 1992 Physiological ecology of ectomycorrhizae: Implications for field application. In Mycorrhizal Functioning. Ed. M FAllen. pp 424–438. Chapman and Hall, New York.Google Scholar
  9. Caldwell M M, Eissenstat D M, Richards J H and Allen M F 1985 Competition for phosphorus: differential uptake from dualisotope-labelled soil interspaces between shrub and grass. Science 229, 384–386.PubMedGoogle Scholar
  10. Clarholm M 1985 Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol. Biochem. 17, 181–187.CrossRefGoogle Scholar
  11. Couteaux M-M, Mousseau M, Celerier M-L and Bottner P 1991 Increased atmospheric CO2 and litter quality: decomposition of sweet chestnut leaf litter with animal food webs of different complexities. Oikos 61, 54–64.Google Scholar
  12. Curtis P S, Drake B G and Whigham D F 1989 Nitrogen and carbon dynamics in C3 and C4 estuarine marsh plants grown under elevated CO2 in situ. Oecologia 78, 297–301.CrossRefGoogle Scholar
  13. Curtis P S, Balduman L M, Drake B G and Whigharn D F 1990 Elevated atmospheric CO2 effects on belowground processes in C3 and C4 estuarine marsh communities. Ecology 71, 2001–2006.CrossRefGoogle Scholar
  14. Diaz S, Grime J P, Harris J and McPherson E 1993 Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364, 616–617.CrossRefGoogle Scholar
  15. Duncan L W and Eissenstat D M 1993 Responses of Tylenchulus semipenetrans to citrus fruit removal: implications for carbohydrate competition. J. Nematol. 25, 7–14.PubMedGoogle Scholar
  16. Fenchel T 1982 Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Marine Ecology Progress Series 8, 225–231.Google Scholar
  17. Fenwick L 1973 Studies on the rhizosphere microflora of onion plants in relationship to temperature changes. Soil Biol. Biochem. 5, 315–320.CrossRefGoogle Scholar
  18. Finn G A and Brun W A 1982 Effect of atmospheric CO2 enrichment on growth, nonstructural carbohydrate content and root nodule activity in soybean. Plant Physiol. 69, 327–331.PubMedGoogle Scholar
  19. Fogel R 1988 Interactions among soil biota in coniferous ecosystems. Agric. Ecosys. Environ. 24, 69–85.CrossRefGoogle Scholar
  20. Fogel R and Hunt G 1979 Fungal and arboreal biomass in a Western Oregon Douglas-fir ecosystem—distribution patterns and turnover. Can. J. For. Res. 9, 245–256.Google Scholar
  21. Fogel R and Hunt G 1983 Contribution of mycorrhizae and soil fungi to nutrient cycling in a Douglas-fir ecosystem. Can. J. For. Res. 13, 219–232.Google Scholar
  22. Freckman D W, Moore J C, Hunt H W and Elliot E T 1991 The effects of elevated CO2 and climate change on soil nematode community structure of prairie sod. Bull. Ecol. Soc. Am. 72 (Suppl.), 119.Google Scholar
  23. Griffiths B and Robinson D 1992 Root-induced nitrogen mineralization: A nitrogen balance model. Plant and Soil 139, 253–263.CrossRefGoogle Scholar
  24. Hardy R W F and Havelka U D 1975 Photosynthate as a major limiting factor limiting nitrogen fixation by field grown legumes with emphasis on soybeans. In Symbiotic Nitrogen Fixation in Plants. Ed. P SNutman. pp 421–439. International Biology Program Series, Vol. 7. Cambridge University Press, London.Google Scholar
  25. Holmes W E and Zak D R 1993 Soil microbial biomass and net nitrogen mineralization in northern hardwood ecosystems. Soil Sci. Soc. Am. J. (In press).Google Scholar
  26. Johnson D W, Ball J T and Walker R F 1994 Effects of elevated CO2 and nitrogen on nutrient uptake in ponderosa pine seedlings. Plant and Soil (In press).Google Scholar
  27. Kelly J M and Beauchamp J J 1987 Mass loss and nutrient dynamics in decomposing oak and mesic mixed-hardwood leaf litter. Soil Sci. Soc. Am. J. 51, 1616–1622.CrossRefGoogle Scholar
  28. Kramer P 1981 Carbon dioxide concentration, photosynthesis, and dry matter production. BioScience 31, 29–33.CrossRefGoogle Scholar
  29. Körner C and Arnone J AIII 1992 Responses to elevated carbon dioxide in artificial tropical ecosystems. Science 257, 1672–1675.PubMedGoogle Scholar
  30. Lamborg M R, Hardy R W F and Paul E A 1983 Microbial effects. In CO2 and Plants. Ed. E RLemon. pp 131–176. AAAS Selected Symposium no. 84. Westview Press, Boulder, Colorado.Google Scholar
  31. Lemon E R 1983 CO2 and Plants. AAAS Selected Symposium No. 84. Westview Press, Boulder, Colorado. 280 p.Google Scholar
  32. Lewis J D, Thomas R B and Strain B R 1992 Interactive effects of nutrient supply and elevated CO2 on response of seedlings from two populations of Pinus taeda to mycorrhizal infection. Bull. Ecol. Soc. Am. 73 (Suppl), 249.Google Scholar
  33. Lewis J D, Thomas R B and Strain B R 1994 Effect of elevated CO2 on mycorrhizal colonization rates of loblolly pine (Pinus taede L.) seedlings. Plant and Soil (This volume).Google Scholar
  34. Lindroth R L and Kinney K K 1993 Effects of atmospheric CO2 and soil NO3 on tree-insect interactions. I. Phytochemical responses. Bull. Ecol. Soc. Am. 74 (Suppl.), 332Google Scholar
  35. Lockwood J L 1981 Exploitation competition. In The Fungal Community: Its Organization and Role in the Ecosystem. Eds. D TWicklow and G CCarroll. pp 319–349. Marcel Dekker, New YorkGoogle Scholar
  36. Luxmoore R J 1981 CO2 and phytomass. BioScience 31, 626.CrossRefGoogle Scholar
  37. Masterson C L and Sherwood M T 1978 Some effects of increased atmospheric carbon dioxide on white clover (Trifolium repens) and pea (Pisum sativum). Plant and Soil 49, 421–426.CrossRefGoogle Scholar
  38. Melillo J M 1983 Will increases in atmospheric concentrations affect litter decay rates? pp 10–11 The Ecosystems Center Annual Report, Marine Biological Laboratory, Woods Hole, Massachusetts, USA.Google Scholar
  39. Monz C A, Hunt H W, Reeves F B and Elliot E T 1994 The response of mycorrhizal colonization to elevated CO2 and climate change in Pascopyrum smithii and Bouteloua gracilis. Plant and Soil (This volume).Google Scholar
  40. Newman E I 1985 The rhizosphere: carbon sources and microbial populations. In Ecological Interactions in Soil: Plants Microbes and Animals. Ed. A HFitter. pp 107–122. London, Blackwell Scientific Publications, London.Google Scholar
  41. Norby R J 1987 Nodulation and nitrogenase activity in nitrogen-fixing woody plants stimulated by CO2 enrichment of the atmosphere. Physiol. Plant. 71, 77–82.CrossRefGoogle Scholar
  42. Norby R J 1994 Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide. Plant and Soil (This volume).Google Scholar
  43. Norby R J, O'Neill E G and Luxmoore R J 1986a Effects of atmospheric CO2 enrichment on the growth and mineral nutrition of Quercus alba in nutrient-poor soil. Plant Physiol. 82, 83–89.PubMedGoogle Scholar
  44. Norby R J, Pastor J and Melillo J M 1986b Carbon-nitrogen interactions in CO2-enriched white oak: physiological and long-term perspectives. Tree Physiol. 2, 233–241.PubMedGoogle Scholar
  45. Norby R J, O'Neill E G and Wullschleger S D 1994 Belowground responses to atmospheric carbon dioxide in forests. In Carbon Forms and Functions in Forest Soils. Eds. W WMcFee and J MKelly. Soil Sci. Soc. of Am. Madison, WI (In press).Google Scholar
  46. Norton J M, Smith J L and Firestone M K 1990 Carbon flow in the rhizosphere of ponderosa pine seedlings. Soil Biol. Biochem. 22, 449–445.CrossRefGoogle Scholar
  47. O'Neill E G and Norby R J 1991 First-year decomposition dynamics of yellow-poplar leaves produced under CO2 enrichment. Bull. Ecol. Soc. Am 72 (Suppl.), 208.Google Scholar
  48. O'Neill E G, Luxmoore R J and R JNorby 1987 Elevated atmospheric CO2 effects on seedling growth, nutrient uptake, and rhizosphere bacterial populations of Liriodendron tulipifera L. Plant and Soil 104, 3–11.CrossRefGoogle Scholar
  49. O'Neill E G, Luxmoore R J and Norby R J 1987 Increases in mycorrhizal colonization and seedling growth in Pinus echinata and Quercus alba in an enriched CO2 atmosphere. Can. J. For. Res. 17, 878–883.Google Scholar
  50. O'Neill E G, O'Neill R V and Norby R J 1991 Hierarchy theory as a guide to mycorrhizal research on large-scale problems. Env. Poll. 73, 271–284.CrossRefGoogle Scholar
  51. Owensby C E, Coyne P I and Auen L M 1993 Nitrogen and phosphorus dynamics of a tallgrass prairie ecosystem exposed to elevated carbon dioxide. Plant Cell Environ. 16, 843–850.CrossRefGoogle Scholar
  52. Phillips D A, Newell K D, Hassell S A and Felling C E 1976 The effect of CO2 enrichment on root nodule development and symbiotic N2 fixation in Pisum sativum L. Am. J. Bot. 63, 356–362.CrossRefGoogle Scholar
  53. Rambelli A 1973 The rhizosphere of mycorrhizae. In Ectomycorrhizae. Eds. G LMarks and T TKozlowski. pp 299–343. Academic Press, New York.Google Scholar
  54. Robinson D, Griffiths B, Ritz K and Wheatley R 1989 Root-induced nitrogen mineralization: A theoretical analysis. Plant and Soil 117, 185–193.CrossRefGoogle Scholar
  55. Rogers H H, Prior S A and O'Neill E G 1992 Cotton root and rhizosphere responses to free-air CO2 enrichment. Crit. Rev. Pl. Sci. 11, 251–263.Google Scholar
  56. Rogers H H, Runion G B and Krupa S V 1993 Plant responses to atmospheric enrichment with emphasis on roots and the rhizosphere. Environ. Poll. (In press).Google Scholar
  57. Rouatt J W and Katznelson H 1960 Influence of light on bacterial flora of roots. Nature 186, 659–660.PubMedCrossRefGoogle Scholar
  58. Rouatt J W, Petersen E A Katznelson H and Henderson V E 1963 Microorganisms in the root zone in relation to temperature. Can. J. Microbiol. 9, 227–236.CrossRefGoogle Scholar
  59. Runion G B, Curl E A, Rogers H H, Backman P A, Rodriguez-Kabana R and Helms B E 1994 Effects of CO2 enrichment on microbial populations in the rhizosphere and phyllosphere of cotton. Agric. For. Met. (In press).Google Scholar
  60. Schwab S M, Leonat R T and Menge J A 1984 Quantitative and qualitative comparison of root exudates of mycorrhizal and non-mycorrhizal plant species. Can. J. Bot. 62, 1227–1231.CrossRefGoogle Scholar
  61. Seastedt T R and Crossley D AJr 1984 The influence of arthropods on ecosystems. BioScience 34, 157–161.CrossRefGoogle Scholar
  62. Strain B R and Bazzaz F A 1983 Terrestrial plant communities. In CO2 and Plants. Ed. E RLemon. pp 177–222. AAAS Selected Symposium no. 84. Westview Press, Boulder, Colorado.Google Scholar
  63. Thomas R B, Richter D D, Ye H, Heine P R and Strain B R 1991 Nitrogen dynamics and growth of seedlings of an N-fixing tree (Gliricidia sepium (Jacq. Walp.)) exposed to elevated atmospheric carbon dioxide. Oecologia 8, 415–421.CrossRefGoogle Scholar
  64. Trappe J M 1977 Selection of mycorrhizal fungi for inoculation in nurseries. Ann. Rev. Phytopath. 15, 203–222.CrossRefGoogle Scholar
  65. Tschaplinski T J and Norby R J 1993 Physiological indicators of nitrogen response in a short rotation sycamore plantation. II. Nitrogen metabolism. Can. J. Bot. 71, 841–847.Google Scholar
  66. vanVeen J A, Liljeroth E, Lekkerkerk L J A Van deGeun S C 1991 Carbon fluxes in plant-soil systems at elevated atmospheric CO2 levels. Ecol. Applic. 1, 175–181.CrossRefGoogle Scholar
  67. Vogt K A, Grier C C and Vogt D J 1986 Production, turnover, and nutrient dynamics of above- and below ground detritus of world forests. Adv. Ecol. Res. 15, 303–377.CrossRefGoogle Scholar
  68. Whipps J M 1985 Effects of CO2 concentration on growth, carbon distribution and loss of carbon from the roots of maize. J. Exp. Bot. 36, 645–651.Google Scholar
  69. Whitbeck J E 1993 Mycorrhizal response to elevated CO2 in serpentine grassland communities. Bull. Ecol. Soc. Am. 74 (Suppl.), 484.Google Scholar
  70. Zak D R, Pregitzer K S, Curtis P, Teeri J A, Fogel R and Randlett D L 1993 Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles in forested ecosystems. Plant and Soil 151, 105–117.Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Elizabeth G. O'Neill
    • 1
  1. 1.Environmental Sciences DivisionOak Ridge National LaboratoryOak RidgeUSA

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