Population Ecology

, Volume 53, Issue 1, pp 35–46 | Cite as

Forest gene diversity is correlated with the composition and function of soil microbial communities

  • Jennifer A. Schweitzer
  • Dylan G. Fischer
  • Brian J. Rehill
  • Stuart C. Wooley
  • Scott A. Woolbright
  • Richard L. Lindroth
  • Thomas G. Whitham
  • Donald R. Zak
  • Stephen C. Hart
Special Feature: Original Article Linking Genome to Ecosystem

Abstract

The growing field of community and ecosystem genetics indicates that plant genotype and genotypic variation are important for structuring communities and ecosystem processes. Little is known, however, regarding the effects of stand gene diversity on soil communities and processes under field conditions. Utilizing natural genetic variation occurring in Populus spp. hybrid zones, we tested the hypothesis that stand gene diversity structures soil microbial communities and influences soil nutrient pools. We found significant unimodal patterns relating gene diversity to soil microbial community composition, microbial exoenzyme activity of a carbon-acquiring enzyme, and availability of soil nitrogen. Multivariate analyses indicate that this pattern is due to the correlation between gene diversity, plant secondary chemistry, and the composition of the microbial community that impacts the availability of soil nitrogen. Together, these data from a natural system indicate that stand gene diversity may affect soil microbial communities and soil processes in ways similar to species diversity (i.e., unimodal patterns). Our results further demonstrate that the effects of plant genetic diversity on other organisms may be mediated by plant functional trait variation.

Keywords

Community and ecosystem genetics Extracellular enzyme activity Functional traits Genetic diversity Populus Unimodal diversity patterns 

References

  1. Bailey JK, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol Lett 9:78–85PubMedGoogle Scholar
  2. Bailey JK, Schweitzer JA, Koricheva J, Madritch MD, LeRoy CJ, Rehill BJ, Bangert RK, Fisher DG, Allen G, Whitham TG (2009) Community and ecosystem consequences of gene flow and genotypic diversity across systems and environments: a meta-analysis. Phil Trans R Soc B 364:1607–1616CrossRefPubMedGoogle Scholar
  3. Barbour RC, O’Reilly-Wapstra JM, De Little DW, Jordan JG, Steane DA, Humphreys JR, Bailey JK, Whitham TG, Potts BM (2009a) Genetic similarity and hierarchical structure within a foundation tree species drives canopy community variation. Ecology 90:1762–1772CrossRefPubMedGoogle Scholar
  4. Barbour BR, Baker SC, O’Reilly-Wapstra JM, Harvest TM, Potts BM (2009b) A footprint of tree genetics on the biota of the forest floor. Oikos 118:1917–1923CrossRefGoogle Scholar
  5. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Per Plant Ecol Evol Syst 7:27–49CrossRefGoogle Scholar
  6. Basaraba J, Starkey RL (1966) Effect of plant tannins on decomposition of organic substances. Soil Sci 101:17–23CrossRefGoogle Scholar
  7. Bending GD, Read DJ (1996) Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1595–1602CrossRefGoogle Scholar
  8. Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity in arbuscular mychorrizal fungi in a mown grassland. J Ecol 84:71–82CrossRefGoogle Scholar
  9. Binkley D, Hart SC (1989) The components of nitrogen availability assessment in forest soils. Adv Soil Sci 10:58–112Google Scholar
  10. Bligh EG, Dwyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917CrossRefGoogle Scholar
  11. Bond EM, Chase JM (2002) Biodiversity and ecosystem functioning and local and regional spatial scales. Ecol Lett 5:467–470CrossRefGoogle Scholar
  12. Bossdorf O, Shuja Z, Banta JA (2009) Genotype and maternal environment affect belowground interactions between Arabidopsis thaliana and its competitors. Oikos 118:1541–1551CrossRefGoogle Scholar
  13. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842CrossRefGoogle Scholar
  14. Chase JM, Leibold MA (2002) Spatial scale dictates the productivity–biodiversity relationship. Nature 416:427–430CrossRefPubMedGoogle Scholar
  15. Clark JS (2010) Individuals and the variation needed for high species diversity in forest trees. Science 327:1129–1132CrossRefPubMedGoogle Scholar
  16. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968CrossRefPubMedGoogle Scholar
  17. Crutsinger GM, Reynolds W, Classen AT, Sanders NJ (2008) Disparate effects of host–plant genotypic diversity on above- and belowground communities. Oecologia 158:65–75CrossRefPubMedGoogle Scholar
  18. Crutsinger GM, Sanders NJ, Classen AT (2009) Comparing intra- and inter-specific variation on litter dynamics. Basic Appl Ecol 10:535–543CrossRefGoogle Scholar
  19. Dang CK, Chauvet E, Gessner MO (2005) Magnitude and variability of process rates in fungal diversity-litter decomposition relationships. Ecol Lett 8:1129–1137CrossRefGoogle Scholar
  20. Diab el Arab HG, Vilich V, Sikora RA (2001) The use of phospholipid fatty acid analysis (PLFA) in the determination of rhizosphere specific microbial communities (RSMC) of two wheat cultivars. Plant Soil 228:291–297CrossRefGoogle Scholar
  21. Diaz S, Hodgson JG, Thompson K, Abido M, Cornelissen JHC, Jalil A, Montserrat-Marti G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Diez P, Prunes G, Hamzehee B, Khoshnevi M, Perez-Harguindeguy N, Perez-Rontome MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martinez M, Romo-Diez A, Shaw S, Siavash B, Villar-Salvador P, Zak MRJ (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304CrossRefGoogle Scholar
  22. Fierer N, Jackson R (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631CrossRefPubMedGoogle Scholar
  23. Fierer N, Grandy NS, Six J, Paul EA (2009) Searching for unifying principles in soil biology. Soil Biol Biochem 41:2249–2256CrossRefGoogle Scholar
  24. Fischer DG, Hart SC, Whitham TG, Martinsen GD, Keim P (2004) Ecosystem implications of genetic variation in water-use of a dominant riparian tree. Oecologia 139:188–197CrossRefGoogle Scholar
  25. Fischer DG, Hart SC, Rehill BJ, Lindroth RL, Keim P, Whitham TG (2006) Do high-tannin leaves require more roots? Oecologia 149:668–675CrossRefPubMedGoogle Scholar
  26. Fischer DG, Hart SC, LeRoy CJ, Whitham TG (2007) Variation in belowground carbon fluxes along a Populus hybridization gradient. New Phytol 176:415–425CrossRefPubMedGoogle Scholar
  27. Fischer DG, Hart SC, Schweitzer JA, Selmants P, Whitham TG (2010) Soil nitrogen availability varies with plant genetics across diverse river drainages. Plant Soil 331:391–400CrossRefGoogle Scholar
  28. Frostegård Å, Bååth E, Tunlid A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:727–730CrossRefGoogle Scholar
  29. Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65CrossRefGoogle Scholar
  30. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. TREE 25:372–380PubMedGoogle Scholar
  31. Grayston SJ, Prescott CE (2005) Microbial communities in forest floors under four tree species in coastal British Columbia. Soil Biol Biochem 37:1157–1167CrossRefGoogle Scholar
  32. Hagerman AE, Butler LG (1989) Choosing appropriate methods and standards for assaying tannin. J Chem Ecol 15:1795–1810CrossRefGoogle Scholar
  33. Hart SC, Firestone MK (1989) Evaluation of three in situ nitrogen availability assays. Can J For Res 19:185–191CrossRefGoogle Scholar
  34. Hart SC, Stark JM, Davidson AE, Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Mickelson SH (ed) Methods of soil analysis, part 2. Soil Science Society of America Book Series, no. 5. Soil Science Society of America, Madison, pp 985–1018Google Scholar
  35. Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. TREE 15:238–243PubMedGoogle Scholar
  36. Hobbie SE (1992) Effects of plant species on nutrient cycling. TREE 7:336–339PubMedGoogle Scholar
  37. Holeski LM, Vogelzang A, Stanosz G, Lindroth RL (2009) Incidence of Venturia shoot blight damage in aspen (Populus tremuloides Michx.) varies with tree chemistry and genotype. Biochem Syst Ecol 37:139–145CrossRefGoogle Scholar
  38. Hooper DU, Bignell EE, Brown VK, Brussaard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, van der Putten WH, de Ruiter PC, Rusek J, Silver WL, Tiedje JM, Wolters V (2000) Interaction between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms and feedbacks. BioScience 50:1049–1061CrossRefGoogle Scholar
  39. Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869–883CrossRefGoogle Scholar
  40. Horner-Devine MC, Leibold MA, Smith VH, Bohannan BJM (2003) Bacterial diversity patterns along a gradient of primary productivity. Ecol Lett 6:613–622CrossRefGoogle Scholar
  41. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623CrossRefPubMedGoogle Scholar
  42. Hughes AR, Stachowicz JJ, Williams SL (2009) Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159:725–733CrossRefPubMedGoogle Scholar
  43. Iason GR, Lennon JJ, Pakeman RJ (2005) Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation? Ecol Lett 8:364–369CrossRefGoogle Scholar
  44. Johnson MTJ, Vellend M, Stinchcombe JR (2009) Evolution in plant populations as a driver of ecological changes in arthropod communities. Phil Trans R Soc B 364:1593–1606CrossRefPubMedGoogle Scholar
  45. Karst J, Jones MD, Turkington R (2009) Ectomycorrhiza colonization and intraspecific variation in growth responses to lodgepole pine. Plant Ecol 200:161–165CrossRefGoogle Scholar
  46. Kasurinen A, Keinänen MM, Kaipainen S (2005) Below-ground response of silver birch trees exposed to elevated CO2 and O3 for three growing seasons. Glob Change Biol 11:1167–1179CrossRefGoogle Scholar
  47. Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256:41–66CrossRefGoogle Scholar
  48. Leckie SE (2005) Methods of microbial community profiling and their application to forest soils. For Ecol Manag 220:88–106CrossRefGoogle Scholar
  49. LeRoy CJ, Whitham TG, Keim P, Marks CJ (2006) Plant genes link forests and streams. Ecology 87:255–261CrossRefPubMedGoogle Scholar
  50. Lojewski NR, Fischer DG, Bailey JK, Schweitzer JA, Whitham TG, Hart SC (2009) Genetic determination of aboveground net primary productivity in a riparian foundation tree species. Tree Physiol 29:1133–1142CrossRefPubMedGoogle Scholar
  51. Madritch M, Donaldson JR, Lindroth RL (2006) Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:528–537CrossRefGoogle Scholar
  52. Madritch MD, Donaldson JR, Lindroth RL (2007) Canopy herbivory mediates the influence of plant genotype on soil processes through frass deposition. Soil Biol Biochem 39:1192–1201CrossRefGoogle Scholar
  53. Madritch MD, Greene SL, Lindroth RL (2009) Genetic mosaics of ecosystem functioning across aspen-dominated landscapes. Oecologia 160:119–127CrossRefPubMedGoogle Scholar
  54. Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L (2001) What is the observed relationship between productivity and diversity? Ecology 82:2381–2396CrossRefGoogle Scholar
  55. Nierop KGJ, Preston CM, Verstraten JM (2006) Linking the B ring hydroxylation pattern of condensed tannins to C, N and P mineralization. A case study using four tannins. Soil Biol Biochem 38:2794–2802CrossRefGoogle Scholar
  56. Northup RR, Dahlgren RA, McColl JG (1998) Polyphenols as regulators of plant–litter–soil interactions in Northern California’s pygmy forest: a positive feedback? Biogeochemistry 42:189–220CrossRefGoogle Scholar
  57. O’Leary WM, Wilkinson SG (1988) Gram positive bacteria. In: Ratlidge C, Wilkinson SG (eds) Microbial lipids, vol 1. Academic, London, pp 117–202Google Scholar
  58. Pastor J, Aber JD, McClaugherty CA, Melillo JM (1984) Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65:256–268CrossRefGoogle Scholar
  59. Paul EA, Clark FE (1996) Soil microbiology and biochemistry, 2nd edn. Elsevier Science, USAGoogle Scholar
  60. Porter LJ, Hrstich LN, Chan BC (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230CrossRefGoogle Scholar
  61. Pregitzer CC, Bailey JK, Hart SC, Schweitzer JA (2010) Soils as agents of selection: feedbacks between plants and soils alter seedling survival and performance. Evol Ecol 24:1045–1059CrossRefGoogle Scholar
  62. Priha OS, Grayston L, Hiukka R, Pennanen T, Smolander A (2001) Microbial community structure and characteristics of the organic matter in soils under Pinus sylvestris, Picea abes and Betula pendula at two forest sites. Biol Fertil Soils 33:17–24CrossRefGoogle Scholar
  63. Reed HE, Martiny JBH (2007) Testing the functional significance of microbial composition in natural communities. FEMS Microbiol Ecol 62:161–170CrossRefPubMedGoogle Scholar
  64. Rehill BJ, Whitham TG, Martinsen GD, Schweitzer JA, Bailey JK, Lindroth RL (2006) Developmental trajectories in cottonwood phytochemistry. J Chem Ecol 32:2269–2285CrossRefPubMedGoogle Scholar
  65. Rhoades C (1997) Single-tree influences on soil properties in agroforestry ecosystems: lessons from natural and savanna ecosystems. Agrofor Syst 35:71–94CrossRefGoogle Scholar
  66. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) Effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  67. Scalbert A (1991) Antimicrobial properties of tannins. Phytochem 30:3875–3883CrossRefGoogle Scholar
  68. Schimel JP, Van Cleve K, Cates RG, Clausen TP, Reichardt PB (1996) Effects of balsam poplar (Populus balsamifera) tannins and low molecular-weight phenolics on microbial activity in tiaga floodplain soil: implications for changes in N cycling during succession. Can J Bot 74:84–90CrossRefGoogle Scholar
  69. Schweitzer JA, Bailey JK, Rehill BJ, Martinsen GD, Hart SC, Lindroth RL, Keim P, Whitham TG (2004) Genetically based trait in a dominant tree affects ecosystem processes. Ecol Lett 7:127–134CrossRefGoogle Scholar
  70. Schweitzer JA, Bailey JK, Hart SC, Wimp GM, Chapman SC, Whitham TG (2005) The interaction of plant genotype and herbivory decelerate leaf litter decomposition and alter nutrient dynamics. Oikos 110:133–145CrossRefGoogle Scholar
  71. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008a) Soil microorganism–plant interactions: heritable relationship between plant genotype and associated microorgansims. Ecology 89:773–781CrossRefPubMedGoogle Scholar
  72. Schweitzer JA, Madritch MD, Bailey JK, LeRoy CJ, Fischer DG, Rehill BJ, Lindroth RL, Hagerman AE, Wooley SC, Hart SC, Whitham TG (2008b) From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005–1020CrossRefGoogle Scholar
  73. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Whitham TG, Hart SC (in press) Functional and heritable consequences of plant genotype on community composition and ecosystem processes. In: Ohgushi T, Schmitz O, Holt R (eds) Ecology and evolution of trait-mediated indirect interactions: linking evolution, community, and ecosystem. Cambridge University Press, CambridgeGoogle Scholar
  74. Shuster SM, Lonsdorf EV, Wimp GM, Bailey JK, Whitham TG (2006) Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60:991–1003PubMedGoogle Scholar
  75. Simchuk A (2008) The effect of fodder plant genotype on the variation of larvalfitness traits in genotype classes of green oak leafroller moth. Russ J Gen 44:418–424CrossRefGoogle Scholar
  76. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  77. Smith KP, Handelsman J, Goodman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci 96:4786–4790CrossRefPubMedGoogle Scholar
  78. Stone AC, Gehring CA, Whitham TG (2010) Drought negatively affects communities on a foundation tree: growth rings predict diversity. Oecologia 164:751–761CrossRefPubMedGoogle Scholar
  79. Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451CrossRefPubMedGoogle Scholar
  80. Swaty RL, Deckert RJ, Whitham TG, Gehring CA (2004) Ectomycorrhizal abundance and community composition shifts with drought: predictions from tree rings. Ecology 85:1072–1084CrossRefGoogle Scholar
  81. Tabatabai MA, Dick WA (2002) Enzymes in soil: research and developments in measuring activities. In: Burns RG, Dick RP (eds) Enzymes in the environment. Marcel Dekker, New York, pp 567–596Google Scholar
  82. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845CrossRefPubMedGoogle Scholar
  83. Treseder KK, Vitousek PM (2001) Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawai’i. Oecologia 126:266–275CrossRefGoogle Scholar
  84. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  85. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846CrossRefGoogle Scholar
  86. Waldrop MP, Zak DR, Sinsabaugh RL, Gallo ME, Lauber CL (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177CrossRefGoogle Scholar
  87. Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135CrossRefPubMedGoogle Scholar
  88. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1634 (a review)CrossRefPubMedGoogle Scholar
  89. Wardle DA, Bardgett RD, Walker LR, Bonner KI (2009) Among- and within-species variation in plant litter decomposition in contrasting long-term chronosequences. Funct Ecol 23:442–453CrossRefGoogle Scholar
  90. Weir BS (1996) Genetic data analysis, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  91. White DC, Davis WM, Nichols JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62CrossRefGoogle Scholar
  92. White DC, Ringleberg DB (1998) Signature lipid biomarker analysis. In: Burlage RS, Atlas R, Stahl D, Gessey G, Sayler G (eds) Techniques in microbial ecology. Oxford University Press, Oxford, pp 255–272Google Scholar
  93. Whitham TG, Young BP, Martinsen GD, Gehring CA, Schweitzer JA, Shuster SM, Wimp GM, Fischer DG, Bailey JK, Lindroth RL, Woolbright SA, Kuske CR (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573CrossRefGoogle Scholar
  94. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf E, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks J, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523CrossRefPubMedGoogle Scholar
  95. Wimp GM, Young WP, Woolbright SA, Martinsen GD, Keim P, Whitham TG (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780CrossRefGoogle Scholar
  96. Wilkinson SG (1988) Gram negative bacteria. In: Ratlidge C, Wilkninson SG (eds) Microbial lipids, vol 1. Academic, London, pp 299–488Google Scholar
  97. Zak DR, Pregitzer KS, Host GE (1986) Landscape variation in nitrogen mineralization and nitrification. Can J For Res 16:1258–1263CrossRefGoogle Scholar
  98. Zak DR, Blackwood CB, Waldrop MP (2006) A molecular dawn for biogeochemistry. TREE 21:288–295PubMedGoogle Scholar
  99. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fert Soils 29:111–129CrossRefGoogle Scholar
  100. Zinke PJ (1962) The pattern of individual forest trees on soil properties. Ecology 43:130–133CrossRefGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer 2010

Authors and Affiliations

  • Jennifer A. Schweitzer
    • 1
  • Dylan G. Fischer
    • 2
  • Brian J. Rehill
    • 3
  • Stuart C. Wooley
    • 4
  • Scott A. Woolbright
    • 5
  • Richard L. Lindroth
    • 6
  • Thomas G. Whitham
    • 5
  • Donald R. Zak
    • 7
  • Stephen C. Hart
    • 8
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  2. 2.Environmental Studies ProgramThe Evergreen State CollegeOlympiaUSA
  3. 3.Department of ChemistryUS Naval AcademyAnnapolisUSA
  4. 4.Department of Biological SciencesCalifornia State University-StanislausTurlockUSA
  5. 5.Department of Biological Sciences, Merriam-Powell Center for Environmental ResearchNorthern Arizona UniversityFlagstaffUSA
  6. 6.Department of EntomologyUniversity of WisconsinMadisonUSA
  7. 7.Department of Ecology and Evolutionary Biology, School of Natural Resources and EnvironmentUniversity of MichiganAnn ArborUSA
  8. 8.School of Natural Sciences, Sierra Nevada Research InstituteUniversity of CaliforniaMercedUSA

Personalised recommendations