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Oecologia

, Volume 186, Issue 1, pp 195–204 | Cite as

Mycorrhizal associations and the spatial structure of an old-growth forest community

  • Daniel J. Johnson
  • Keith Clay
  • Richard P. Phillips
Community ecology – original research

Abstract

Plant-soil feedbacks are known to play a central role in species co-existence, but conceptual frameworks for predicting their magnitude and direction are lacking. We ask whether co-occurring trees that associate with different types of mycorrhizal fungi, which are hypothesized to differ in terms of nutrient use and plant-soil feedbacks, differ in sapling establishment densities and probability of co-occurrence. Given that ectomycorrhizal (ECM) trees typically have fungal structures that protect roots from pathogens whereas arbuscular mycorrhizal (AM) trees do not, we hypothesized that ECM saplings would be clustered around ECM trees, while AM saplings would be suppressed near AM trees. Most previous studies have focused on seedlings, but here we examine whether the spatial signal is evident in later life stages. We measured the spatial associations of ~ 28,000 trees using point pattern analysis in a 25-ha old-growth forest where ECM trees comprised 72% of total basal area and 42% of the total stems, while AM trees comprised the remainder. Supporting our hypothesis, AM saplings were more inhibited by AM trees, while ECM saplings were more clustered around ECM trees. The spatial patterns of AM and ECM trees on saplings of the alternate mycorrhizal type were inhibited. To the extent that similar types of feedbacks occur for other AM and ECM trees, our results suggest that fundamental differences in the nature of local-scale biotic interactions between trees and their fungal symbionts may influence forest community assembly and ecosystem dynamics.

Keywords

Arbuscular mycorrhizae Ectomycorrhizae Oak–hickory forest Pair-correlation function ForestGEO 

Notes

Acknowledgements

Thanks to field crew members J. Degler, A. Quebbeman, M. Sheehan, A. Sipes and the dozens of volunteers that helped maintain the IUFDP. Thanks to R. Condit and S. Lao of the Smithsonian Institution for assistance with data curation. Funding for the plot establishment was provided by a National Science Foundation (NSF) Doctoral Dissertation Improvement Grant (1110533) to DJJ and KC, Indiana University Research and Teaching Preserves, Indiana Academy of Science and the Smithsonian Tropical Research Institute. Portions of this work benefited from ForestGEO workshops attended by DJJ (NSF Division of Environmental Biology—1046113 to S. J. Davies).

Author contribution statement

DJJ, KC and RPP conceived of the idea. DJJ supervised the data collection, performed the analyses, and wrote the initial draft. All authors wrote and edited the manuscript.

Supplementary material

442_2017_3987_MOESM1_ESM.pdf (402 kb)
Supplementary material 1 (PDF 401 kb)

References

  1. Anderson-Teixeira KJ et al (2015) CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob Change Biol 21:528–549. doi: 10.1111/gcb.12712 CrossRefGoogle Scholar
  2. Bâ AM, McGuire KL, Diédhiou AG (2014) Ectomycorrhizal symbioses in tropical and neotropical forests. CRC, Boca RatonGoogle Scholar
  3. Baddeley A, Turner R (2005) spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12:42. doi: 10.18637/jss.v012.i06 CrossRefGoogle Scholar
  4. Baddeley AJ, Møller J, Waagepetersen R (2000) Non- and semi-parametric estimation of interaction in inhomogeneous point patterns. Stat Neerl 54:329–350. doi: 10.1111/1467-9574.00144 CrossRefGoogle Scholar
  5. Baddeley A, Rubak E, Turner R (2015) Spatial point patterns. CRC, Boca RatonGoogle Scholar
  6. Bauer JT, Mack KML, Bever JD (2015) Plant-soil feedbacks as drivers of succession: evidence from remnant and restored tallgrass prairies. Ecosphere 6:1–12. doi: 10.1890/ES14-00480.1 CrossRefGoogle Scholar
  7. Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. doi: 10.1126/science.aai8212 CrossRefPubMedGoogle Scholar
  8. Bever JD, Mangan SA, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325. doi: 10.1146/annurev-ecolsys-112414-054306 CrossRefGoogle Scholar
  9. Burrascano S, Keeton WS, Sabatini FM, Blasi C (2013) Commonality and variability in the structural attributes of moist temperate old-growth forests: a global review. For Ecol Manage 291:458–479. doi: 10.1016/j.foreco.2012.11.020 CrossRefGoogle Scholar
  10. Chapman SK, Langley JA, Hart SC, Koch GW (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34. doi: 10.1111/j.1469-8137.2005.01571.x CrossRefPubMedGoogle Scholar
  11. Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332CrossRefPubMedGoogle Scholar
  12. Condit R (1998) Tropical forest census plots: methods and results from Barro Colorado Island, Panama and a comparison with other plots. Springer, New YorkCrossRefGoogle Scholar
  13. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forests. In: den Boer PJG, Gradwells GR (eds) Dynamics of populations. Center for Agricultural Publishing and Documentation, Wageningen, pp 298–310Google Scholar
  14. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  15. Cornelissen JHC, Aerts R, Cerabolini B, Werger MJA, van der Heijden MGA (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129:611–619CrossRefPubMedGoogle Scholar
  16. Corrales A, Mangan SA, Turner BL, Dalling JW (2016) An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol Lett 19:383–392CrossRefPubMedGoogle Scholar
  17. de Kroon H et al (2012) Root responses to nutrients and soil biota: drivers of species coexistence and ecosystem productivity. J Ecol 100:6–15. doi: 10.1111/j.1365-2745.2011.01906.x CrossRefGoogle Scholar
  18. Development Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  19. Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany 92:149–160. doi: 10.1139/cjb-2013-0091 CrossRefGoogle Scholar
  20. Getzin S, Wiegand T, Wiegand K, He F (2008) Heterogeneity influences spatial patterns and demographics in forest stands. J Ecol 96:807–820. doi: 10.1111/j.1365-2745.2008.01377.x CrossRefGoogle Scholar
  21. Goebel PC, Hix DM (1996) Development of mixed-oak forests in southeastern Ohio: a comparison of second-growth and old-growth forests. For Ecol Manage 84:1–21. doi: 10.1016/0378-1127(96)03772-3 CrossRefGoogle Scholar
  22. Harms KE, Wright SJ, Calderón O, Hernández A, Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495CrossRefPubMedGoogle Scholar
  23. Hersh MH, Vilgalys R, Clark JS (2012) Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival. Ecology 93:511–520. doi: 10.1890/11-0598.1 CrossRefPubMedGoogle Scholar
  24. Holste EK, Kobe RK, Gehring CA (2017) Plant species differ in early seedling growth and tissue nutrient responses to arbuscular and ectomycorrhizal fungi. Mycorrhiza 27:211–223. doi: 10.1007/s00572-016-0744-x CrossRefPubMedGoogle Scholar
  25. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  26. Jastrow J (1996) Soil aggregate formation and the accrual of particulate and mineral-associated organic matter. Soil Biol Biochem 28:665–676CrossRefGoogle Scholar
  27. Jenkins JC, Chojnacky DC, Heath LS, Birdsey RA (2003) National-scale biomass estimators for United States tree species. For Sci 49:12–35Google Scholar
  28. Johnson DJ, Beaulieu WT, Bever JD, Clay K (2012) Conspecific negative density dependence and forest diversity. Science 336:904–907. doi: 10.1126/science.1220269 CrossRefPubMedGoogle Scholar
  29. Johnson DJ, Bourg NA, Howe R, McShea WJ, Wolf A, Clay K (2014) Conspecific negative density-dependent mortality and the structure of temperate forests. Ecology 95:2493–2503. doi: 10.1890/13-2098.1 CrossRefGoogle Scholar
  30. Kardol P, Martijn Bezemer T, van der Putten WH (2006) Temporal variation in plant–soil feedback controls succession. Ecol Lett 9:1080–1088. doi: 10.1111/j.1461-0248.2006.00953.x CrossRefPubMedGoogle Scholar
  31. Kulmatiski A, Beard KH, Heavilin J (2012) Plant–soil feedbacks provide an additional explanation for diversity–productivity relationships. Proc R Soc B Biol Sci. doi: 10.1098/rspb.2012.0285 Google Scholar
  32. LaManna JA, Walton ML, Turner BL, Myers JA (2016) Negative density dependence is stronger in resource-rich environments and diversifies communities when stronger for common but not rare species. Ecol Lett 19:657–667. doi: 10.1111/ele.12603 CrossRefPubMedGoogle Scholar
  33. LaManna JA et al (2017) Plant diversity increases with the strength of negative density dependence at the global scale. Science 356:1389–1392. doi: 10.1126/science.aam5678 CrossRefPubMedGoogle Scholar
  34. Lin G, McCormack ML, Ma C, Guo D (2016) Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol 213:1440–1451. doi: 10.1111/nph.14206 CrossRefPubMedGoogle Scholar
  35. Marx DH (1972) Ectomycorrhizae as biological deterrents to pathogenic root infections. Annu Rev Phytopathol 10:429–454. doi: 10.1146/annurev.py.10.090172.002241 CrossRefPubMedGoogle Scholar
  36. McCarthy-Neumann S, Ibáñez I (2012) Tree range expansion may be enhanced by escape from negative plant–soil feedbacks. Ecology 93:2637–2649. doi: 10.1890/11-2281.1 CrossRefPubMedGoogle Scholar
  37. McGuire KL (2007) Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567–574. doi: 10.1890/05-1173 CrossRefPubMedGoogle Scholar
  38. McIntire EJB, Fajardo A (2009) Beyond description: the active and effective way to infer processes from spatial patterns. Ecology 90:46–56CrossRefPubMedGoogle Scholar
  39. McNab WH, Cleland DT, Freeouf JA, Keys JEJ, Nowacki G.J., Carpenter CA (2007) Description of ecological subregions: sections of the conterminous United States. In: U.S. Department of Agriculture FS (ed), vol. Gen. Tech. Report WO-76B, [CD-ROM] edn, Washington, D.C., p 80Google Scholar
  40. Mead R (1966) A relationship between individual plant-spacing and yield. Ann Bot 30:301–309CrossRefGoogle Scholar
  41. Midgley MG, Brzostek E, Phillips RP (2015) Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees. J Ecol 103:1454–1463. doi: 10.1111/1365-2745.12467 CrossRefGoogle Scholar
  42. Oksanen J et al (2015) vegan: Community Ecology PackageGoogle Scholar
  43. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281CrossRefPubMedGoogle Scholar
  44. Parker GR (1989) Old-growth forests of the central hardwood region. Nat Areas J 9:5–11Google Scholar
  45. Parker GR, Leopold DJ, Eichenberger JK (1985) Tree dynamics in an old-growth, deciduous forest. For Ecol Manage 11:31–57CrossRefGoogle Scholar
  46. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51. doi: 10.1111/nph.12221 CrossRefPubMedGoogle Scholar
  47. Pierce AR, Parker G, Rabenold K (2006) Forest succession in an Oak-Hickory dominated stand during a 40-year period at the Ross Biological Reserve, Indiana. Nat Areas J 26:351–359. doi:10.3375/0885-8608(2006)26[351:FSIAOD]2.0.CO;2Google Scholar
  48. Purves D, Pacala S (2008) Predictive models of forest dynamics. Science 320:1452–1453. doi: 10.1126/science.1155359 CrossRefPubMedGoogle Scholar
  49. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492. doi: 10.1046/j.1469-8137.2003.00704.x CrossRefGoogle Scholar
  50. Reinhart KO, Packer A, Van der Putten WH, Clay K (2003) Plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:1046–1050. doi: 10.1046/j.1461-0248.2003.00539.x CrossRefGoogle Scholar
  51. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291. doi: 10.1890/02-0298 CrossRefGoogle Scholar
  52. Rhynsburger D (1973) Analytic delineation of Thiessen polygons. Geogr Anal 5:133–144. doi: 10.1111/j.1538-4632.1973.tb01003.x CrossRefGoogle Scholar
  53. Runkle JR (2012) Thirty-two years of change in an old-growth Ohio beech–maple forest. Ecology 94:1165–1175. doi: 10.1890/11-2199.1 CrossRefGoogle Scholar
  54. Schmelz DV, Alton AL (1970) Relationship among the forest types of Indiana. Ecology 51:620–629. doi: 10.2307/1934041 CrossRefGoogle Scholar
  55. Schmelz DV, Lindsey AA (1965) Size-class structure of old-growth forests in Indiana. For Sci 11:258–264Google Scholar
  56. Shotola SJ, Weaver GT, Robertson PA, Ashby WC (1992) Sugar maple invasion of an old-growth oak-hickory forest in southwestern Illinois. Am Midl Nat 127:125–138. doi: 10.2307/2426328 CrossRefGoogle Scholar
  57. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press-Elsevier, Amsterdam, The NetherlandsGoogle Scholar
  58. Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16. doi: 10.2307/1939377 CrossRefGoogle Scholar
  59. Van Der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150. doi: 10.1111/j.1365-2745.2009.01570.x CrossRefGoogle Scholar
  60. Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62. doi: 10.1016/j.soilbio.2011.11.018 CrossRefGoogle Scholar
  61. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. doi: 10.1007/s00572-005-0033-6 CrossRefPubMedGoogle Scholar
  62. Wang X, Wiegand T, Hao Z, Li B, Ye J, Lin F (2010) Species associations in an old-growth temperate forest in north-eastern China. J Ecol 98:674–686. doi: 10.1111/j.1365-2745.2010.01644.x CrossRefGoogle Scholar
  63. Waring BG, Adams R, Branco S, Powers JS (2016) Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytol 209:845–854CrossRefPubMedGoogle Scholar
  64. Wiegand T, Moloney KA (2004) Rings, circles, and null-models for point pattern analysis in ecology. Oikos 104:209–229CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Daniel J. Johnson
    • 1
  • Keith Clay
    • 2
  • Richard P. Phillips
    • 2
  1. 1.Utah State UniversityLoganUSA
  2. 2.Indiana UniversityBloomingtonUSA

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