, Volume 11, Issue 6, pp 1005–1020 | Cite as

From Genes to Ecosystems: The Genetic Basis of Condensed Tannins and Their Role in Nutrient Regulation in a Populus Model System

  • Jennifer A. Schweitzer
  • Michael D. Madritch
  • Joseph K. Bailey
  • Carri J. LeRoy
  • Dylan G. Fischer
  • Brian J. Rehill
  • Richard L. Lindroth
  • Ann E. Hagerman
  • Stuart C. Wooley
  • Stephen C. Hart
  • Thomas G. Whitham


Research that connects ecosystem processes to genetic mechanisms has recently gained significant ground, yet actual studies that span the levels of organization from genes to ecosystems are extraordinarily rare. Utilizing foundation species from the genus Populus, in which the role of condensed tannins (CT) has been investigated aboveground, belowground, and in adjacent streams, we examine the diverse mechanisms for the expression of CT and the ecological consequences of CT for forests and streams. The wealth of data from this genus highlights the importance of form and function of CT in large-scale and long-term ecosystem processes and demonstrates the following four patterns: (1) plant-specific concentration of CT varies as much as fourfold among species and individual genotypes; (2) large within-plant variation in CT occurs due to ontogenetic stages (that is, juvenile and mature), tissue types (that is, leaves versus twigs) and phenotypic plasticity in response to the environment; (3) CT have little consistent effect on plant–herbivore interactions, excepting organisms utilizing woody tissues (that is, fungal endophytes and beaver), however; (4) CT in plants consistently slow rates of leaf litter decomposition (aquatic and terrestrial), alter the composition of heterotrophic soil communities (and some aquatic communities) and reduce nutrient availability in terrestrial ecosystems. Taken together, these data suggest that CT may play an underappreciated adaptive role in regulating nutrient dynamics in ecosystems. These results also demonstrate that a holistic perspective from genes-to-ecosystems is a powerful approach for elucidating complex ecological interactions and their evolutionary implications.


above- and belowground interactions aquatic–terrestrial linkages condensed tannin community genetics Populus plant–soil feedbacks Salicaceae 


  1. Ardon M, Stallcup LA, Pringle CM. 2006. Does leaf quality mediate the stimulation of leaf breakdown by phosphorus in neotropical streams? Freshwater Biology 51: 618–33.Google Scholar
  2. Arnold TM, Schultz JC. 2002. Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130: 585–93.Google Scholar
  3. Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J. 2004. Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink–source model of plant defense. New Phytol 164: 157–64.Google Scholar
  4. Athanasiadou S, Kyriazakis I. 2004. Plant secondary metabolites: Antiparasitic effects and their role in ruminant production systems. Proceedings of Nutrition Society 63: 631–9.PubMedGoogle Scholar
  5. Ayres MP, Clausen TP, MacLean Jr. SF, Redman AM, Reichardt PB. 1997. Diversity of structure and anti-herbivore activity in condensed tannins. Ecology 78: 1696–712.Google Scholar
  6. Bailey JK, Schweitzer JA, Martinsen GD, Howe MA, Whitham TG. 2002. Beaver preference and plant species shifts: implications for exotic invasions. In: Proceedings from the 11th international conf. of exotic invasions of aquatic systems, pp 180–8Google Scholar
  7. Bailey JK, Schweitzer JA, Rehill BJ, Lindroth RL, Keim P, Whitham TG. 2004. Beavers as molecular geneticists: A genetic basis to the foraging of an ecosystem engineer. Ecology 85: 603–8.Google Scholar
  8. Bailey JK, Deckert R, Schweitzer JA, Rehill BJ, Lindroth RL, Gehring C, Whitham TG. 2005. Host-plant genetics affect hidden ecological players: Links among Populus, condensed tannins and fungal endophyte infection. Can J Bot 83: 356–62.Google Scholar
  9. 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: 78–85.PubMedGoogle Scholar
  10. Bailey JK, Irschick DJ, Schweitzer JA, Rehill BJ, Lindroth RL, Whitham TJ. 2007. Selective herbivory by elk results in rapid shifts in the chemical composition of aspen forests. Biological Invasions 9: 715–22.Google Scholar
  11. Bangert RK, Turek RJ, Rehill BJ, Wimp GM, Schweitzer JA, Allan GJ, Bailey JK, Martinsen GD, Keim P, Lindroth RL, Whitham TG. 2006. A genetic similarity rule determines arthropod community structure. Mol Ecol 15: 1379–91.PubMedGoogle Scholar
  12. Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen J-P. 2006. Ellagitannins have greater oxidative activites than condensed tannins and galloyl glucoses at high pH: Potential impact on caterpillars. J Chem Ecol 32: 2253–67.PubMedGoogle Scholar
  13. Basaraba J, Starkey RL. 1966. Effect of plant tannins on decomposition of organic substances. Soil Sci 101: 17–23.Google Scholar
  14. Basey JM, Jenkins SH, Busher PE. 1988. Optimal central-place foraging by beavers: Tree-size selection in relation to defensive chemicals of quaking aspen. Oecologia 76: 278–82.Google Scholar
  15. Bending GD, Read DJ. 1996. Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28: 1595–602.Google Scholar
  16. Bhat TK, Singh B., Sharma OP. 1998. Microbial degradation of tannins—A current perspective. Biodegradation 9:343–57.PubMedGoogle Scholar
  17. Benoit RE, Starkey RL. 1968. Inhibition of decomposition of cellulose and some other carbohydrates by tannin. Soil Sci 105: 291–6.CrossRefGoogle Scholar
  18. Bernays EA, Cooper DG, Bilgener M. 1989. Herbivores and plant tannins. In: Begon M, Fitter AH, Ford ED, MacFadyen A, Eds. Advances in ecological research, vol 19. London: Academic Press. pp 263–302Google Scholar
  19. Binkley D, Giardina C. 1998. Why do tree species affect soils? The Warp and Woof of tree-soil interactions. Biogeochemistry 42: 89–106.Google Scholar
  20. Bradley RL, Titus BD, Preston CP. 2000. Changes to mineral N cycling and microbial communities in black spruce humus after additions of (NH4)2SO4 and condensed tannins extracted from Kalmia angustifolia and balsam fir. Soil Biol Biochem 32:1227–40.Google Scholar
  21. Bryant JP, Chapin III S, Klein DR. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357–68.Google Scholar
  22. Butler LG. 1989. Effects of condensed tannin on animal nutrition. In: Hemingway RW, Karchesy JJ, Eds. Chemistry and significance of condensed tannins. NY: Plenum Press. pp 391–416Google Scholar
  23. Campbell IC, Fuchshuber L. 1995. Polyphenols, condensed tannins, and processing rates of tropical and temperate leaves in an Australian stream. Journal of the North American Benthological Society 14: 174–82.Google Scholar
  24. Castells E, Peñuelas J, Valentine DW. 2004. Are phenolic compounds released from the Mediterranean shrub Cistus albidus responsible for change in N cycling in sileceous and calcerious soils? New Phytol 162:187–95.Google Scholar
  25. Cates RG, Rhoades DF. 1977. Patterns in the production of antiherbivore chemical defenses in plant communities. Biochem Syst Ecol 5: 185–93.Google Scholar
  26. Chapman SC, Schweitzer JA, Whitham TG. 2006. Herbivory differentially alters plant litter dynamics of evergreen and deciduous trees. Oikos 114: 566–74.Google Scholar
  27. Choudhury D. 1988. Herbivore induced changes in leaf-litter resource quality: A neglected aspect of herbivory in ecosystem nutrient dynamics. Oikos 51: 389–93.Google Scholar
  28. Clausen TP, Provenza FD, Burritt EA, Reichard PB, Bryant JP. 1990. Ecological implications of condensed tannin structure: A case study. J Chem Ecol 16: 2381–92.Google Scholar
  29. Clein JS, Schimel JP. 1995. Nitrogen turnover and availability during succession from alder to poplar in Alaskan taiga forests. Soil Biol Biochem 27: 743–52.Google Scholar
  30. Close DC, McArthur C. 2002. Rethinking the role of many plant phenolics—protection from photodamage not herbivores? Oikos 99: 166–72.Google Scholar
  31. Conner JK, Hartl DL. 2004. A Primer of Ecological Genetics. Sinauer, Sunderland.Google Scholar
  32. Dalzell SA, Shelton SM. 2002. Genotypic variation in proanthocyanidin status of Leucaena genus. J Agric Sci 138: 209–20.Google Scholar
  33. Dixon RA, Xie DY, Sharma SB. 2005. Proanthocyanidins—a final frontier in flavinoid research? New Phytol 165: 9–28.PubMedGoogle Scholar
  34. Donaldson JR, Lindroth RL. 2004. Cottonwood leaf beetle (Coleoptera: Chrysomelidae) performance in relation to variable phytochemistry in juvenile aspen (Populus tremuloides Michx.). Environ Entomol 33: 1505–11.CrossRefGoogle Scholar
  35. Donaldson JR, Lindroth RL. 2007. Genetics, environment, and G × E interactions determine efficacy of chemical defense in trembling aspen. Ecology 88: 729–39.PubMedGoogle Scholar
  36. Donaldson JR, Stevens MT, Barnhill HR, Lindroth RL. 2006. Age-related shifts in leaf chemistry of clonal aspen. J Chem Ecol 32: 1415–29.PubMedGoogle Scholar
  37. Driebe EM, Whitham TG. 2000. Cottonwood hybridization affects tannin and nitrogen of leaf litter and alters decomposition. Oecologia 123: 99–107.Google Scholar
  38. Dungey HS, Potts BM, Whitham TG, Li H.-L. 2000. Plant genetics affects arthropod community richness and composition: Evidence from a synthetic eucalypt hybrid population. Evolution 54: 1938–46.PubMedGoogle Scholar
  39. Fahey Jr GC, Jung HG. 1989. Phenolic compounds in forages and fibrous feedstuffs. In: Cheeke PR, Ed. Toxicants of plant origin, vol IV, Phenolics. Florida: CRC Press, Inc. pp 123–90Google Scholar
  40. Feeny PP. 1968. Effect of oak leaf tannins on larval growth of the winter moth Operopthera brumata. J Insect Physiol 14: 805–17.Google Scholar
  41. Feeny PP. 1969. Inhibitory effects of oak leaf tannins on the hydrolysis of trypsin. Phytochemistry 8:2119–26.Google Scholar
  42. Feeny PP. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51: 565–81.Google Scholar
  43. Field JA, Lettinga G 1992. Toxicity of tannic compounds to microorganisms. Hemingway RW, Laks PE, editors. Plant Polyphenols. Synthesis, Properties, Significance. Plenum Press, New York. pp. 673–92.Google Scholar
  44. Fierer N, Schimel JP, Cates RG, Zou Z. 2001. The influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33: 1827–39.Google Scholar
  45. Findlay S, Carreiro M, Krischik V, Jones CG. 1996. Effects of damage to living plants on leaf litter quality. Ecol Appl 6: 269–75.Google Scholar
  46. Fischer DG, Hart SC, Rehill BJ, Lindroth RL, Keim P, Whitham TG. 2006. Do high tannin leaves require more roots? Oecologia 149:668–75.PubMedGoogle Scholar
  47. Fischer DG, Hart SC, LeRoy CJ, Whitham TG. 2007. Variation in below-ground carbon fluxes along a Populus hybridization gradient. New Phytol 176: 415–25.PubMedGoogle Scholar
  48. Forkner RE, Marquis RJ, Lill JT. 2004. Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29:174–87.Google Scholar
  49. Gallardo A, Merino J. 1992. Nitrogen immobilization in leaf litter at two mediterranean ecosystems of SW Spain. Biogeochemistry 15: 213–28.Google Scholar
  50. Gehring CA, Mueller RC, Whitham TG. 2006. Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149:158–64.PubMedGoogle Scholar
  51. Hagerman AE. 1992. Tannin–Protein Interactions. ACS Symposium Series 506: 236–47.CrossRefGoogle Scholar
  52. Hagerman AE, Robbins CT, Weerasuriya Y, Wilson TC, McArthur C. 1992. Tannin chemistry in relation to digestion. Journal of Range Management 45:57–62.Google Scholar
  53. Harding SA, Jiang H, Jeong ML, Casado FL, Lin H-W, Tsai C-J. 2005. Functional genomics analysis of foliar condensed tannin and phenolic glycoside regulation in natural cottonwood hybrids. Tree Physiol 25: 1475–86.PubMedGoogle Scholar
  54. Haslam E. 1988. Plant polyphenols (syn. vegetable tannins) and chemical defense—a reappraisal. J Chem Ecol 14: 1789–806.Google Scholar
  55. Hättenschwiler S, Vitousek PM. 2000. The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15: 238–43.PubMedGoogle Scholar
  56. Hättenschwiler S, Tiunov AI, Scheu S. 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Evolution and Systematics 36: 191–218.Google Scholar
  57. Havill NP, Raffa KF. 1999. Effects of eliciting treatment and genotypic variation on induced resistance in Populus: Impacts on gypsy moth development and feeding behavior. Oecologia 120: 295–303.Google Scholar
  58. Hemming JDC, Lindroth RL. 1995. Intraspecific variation in aspen phytochemistry: effects on performance of gypsy moths and forest tent caterpillars. Oecologia 103: 79–88.Google Scholar
  59. Holton MK, Lindroth RL, Nordheim EV. 2003. Foliar quality influences tree–herbivore–parasitoid interactions: Effects of CO2, O3 and plant genotype. Oecologia 137: 233–44.PubMedGoogle Scholar
  60. Horner JD, Gosz JR, Cates RG. 1988. The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. American Naturalist 132: 869–83.Google Scholar
  61. Hunter MD. 2001. Insect population dynamics meets ecosystem ecology: Effects of herbivory on soil nutrient dynamics. Agricultural Forest Entomology 3: 77–84.Google Scholar
  62. Hwang S-Y, Lindroth RL. 1997. Clonal variation in foliar chemistry of aspen: Effects on gypsy moths and forest tent caterpillars. Oecologia 111: 99–108.Google Scholar
  63. Hwang S-Y, Lindroth RL. 1998. Consequences of clonal variation in aspen phytochemistry for late season folivores. Écoscience 5: 508–16.Google Scholar
  64. Iason GR, Vilalba JJ. 2006. Behavioral strategies of mammal herbivores against plant secondary compounds: The avoidance-tolerance continuum. J Chem Ecol 32: 1115–32.PubMedGoogle Scholar
  65. Kanerva S, Kitunen V, Kiikkilä O, Loponen J, Smolander A. 2006. Response of soil C and N transformations to tannin fractions originating from Scots pine and Norway spruce needles. Soil Biol Biochem 38: 1364–74.Google Scholar
  66. Kasurinen A, Keinänen MM, Kaipainen S, Nilsson L-O, Vapaavuori E, Kontro MH, Holopainen T. 2005. Below-ground response of silver birch trees exposed to elevated CO2 and O3 for three growing seasons. Global Change Biology 11: 1167–79.Google Scholar
  67. Kearsley MJC, Whitham TG. 1998. The developmental stream of cottonwoods affects ramet growth and resistance to herbivory by galling aphids. Ecology 79: 178–91.Google Scholar
  68. Kosola KR, Parry D, Workmaster BAA. 2006. Responses of condensed tannin in Poplar roots to fertilization and gypsy moth defoliation. Tree Physiol 26: 1607–11.PubMedGoogle Scholar
  69. Kraus TEC, Dahlgren RA, Zasoski RJ. 2003. Tannins in nutrient dynamics of forest ecosystems—a review. Plant and Soil 256: 41–66.Google Scholar
  70. Kraus TEC, Zasoski RJ, Dahlgren RA, Horwath WR, Preston CM. 2004. Carbon and nitrogen dynamics in a forest soil amended with purified tannins from different plant species. Soil Biol Biochem 36: 309–21.Google Scholar
  71. Lawrence R, Potts BM, Whitham TG. 2003. Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84: 1171–8.Google Scholar
  72. LeRoy CJ, Whitham TG, Keim P, Marks JC. 2006. Plant genes link forests and streams. Ecology 87: 255–61.PubMedGoogle Scholar
  73. LeRoy CJ, Wooley SC, Whitham TG, Marks JC. 2007. Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river. Journal of the North American Benthological Society 26: 426–38.Google Scholar
  74. Lindroth RL, Hwang S-Y. 1996. Clonal variation in foliar chemistry of quaking aspen (Populus tremuloides Michx.). Biochem Syst Ecol 24: 357–64.Google Scholar
  75. Lindroth RL, Kinney KK, Platz CL. 1993. Responses of deciduous trees to elevated atmospheric CO2: Productivity, phytochemistry and insect performance. Ecology 74: 763–77.Google Scholar
  76. Lindroth RL, Roth S, Kruger EL, Volin JC, Koss PA. 1997. CO2-mediated changes in aspen chemistry: Effects on gypsy moth performance and susceptibility to virus. Global Change Biology 3: 279–89.Google Scholar
  77. Lindroth RL, Donaldson JR, Stevens MT, Gusse AC. 2007. Browse quality in quaking aspen (Populus tremuloides): effects of genotype, nutrients, defoliation, and coppicing. J Chem Ecol 33; 1049–64.PubMedGoogle Scholar
  78. Liu L, King JS, Giardina CP. 2005. Effects of elevated concentrations of atmospheric CO2 and tropospheric O3 on leaf litter production and chemistry in trembling aspen and paper birch communities. Tree Physiol 25: 1511–22.PubMedGoogle Scholar
  79. Lowjewski NR. 2007. Genetic determination of aboveground net primary productivity in a riparian foundation tree species. Master’s Thesis, Northern Arizona UniversityGoogle Scholar
  80. Madritch MD, Hunter MD. 2002. Phenotypic diversity influences ecosystem functioning in an oak sandhills community. Ecology 83: 2084–90.Google Scholar
  81. Madritch MD, Donaldson JR, Lindroth RL. 2006. Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9: 528–37.Google Scholar
  82. Madritch MD, Donaldson JR, Lindroth RL. 2007a. Canopy herbivory can mediate the influence of plant genotype on soil processes through frass deposition. Soil Biol Biochem 39:1192–201.Google Scholar
  83. Madritch MD, Jordan LM, Lindroth RL. 2007b. Interactive effects of condensed tannin and cellulose additions on soil respiration. Canadian Journal of Forest Research 37:2063–7.Google Scholar
  84. Mansfield JL, Curtis PS, Zak DR, Pregitzer KS. 1999. Genotypic variation for condensed tannin production in trembling aspen (Populus tremuloides, Salicaceae) under elevated CO2 and in high- and low-fertility soil. American Journal of Botanty 86: 1154–9.PubMedGoogle Scholar
  85. Marles MAS, Ray H, Gruber MY. 2003. New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry 64: 357–83.Google Scholar
  86. 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: 2794–802.Google Scholar
  87. 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: 189–220.Google Scholar
  88. Nykänen H, Koricheva J. 2004. Damage-induced changes in woody plants and their effects on insect herbivore performance: A meta-analysis. Oikos 104: 247–68.Google Scholar
  89. O’Reilly-Wapastra JM, Potts BM, McArthur C, Davies NW, Tilyard P. 2005. Inheritance of resistance to mammalian herbivores and of plant defensive chemistry in a Eucalytpus species. J Chem Ecol 31: 357–75.Google Scholar
  90. Osier TL, Lindroth RL. 2001. Effects of genotype, nutrient availability and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27: 1289–313.PubMedGoogle Scholar
  91. Osier TL, Lindroth RL. 2004. Long-term effects of defoliation on quaking aspen in relation to genotype and nutrient availability: Plant growth, phytochemistry and insect performance. Oecologia 139: 55–65.PubMedGoogle Scholar
  92. Osier TL, Lindroth RL. 2006. Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148: 293–303.PubMedGoogle Scholar
  93. Ostrofsky ML. 1997. Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. Journal of the North American Benthological Society 16: 750–9.Google Scholar
  94. Palm CA, Sanchez PA. 1991. Nitrogen release from the leaves of some tropical legumes as affected by their lignin and polyphenolic contents. Soil Biol Biochem 23: 83–88.Google Scholar
  95. Peters DJ, Constabel JP. 2002. Molecular analysis of herbivore-induced condensed tannin synthesis: Cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant Journal 32: 701–12.PubMedGoogle Scholar
  96. Ralph S, Oddy C, Cooper D, others. 2006. Genomics of hybrid poplar (Populus trichocarpa × P. deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15:1275–97Google Scholar
  97. Rehill BJ, Clauss A., Wieczorek L., Whitham TG, Lindroth RL. 2005. Foliar phenolic glycosides from Populus fremontii, Populus angustifolia, and their hybrids. Biochemical Systematics and Ecology 33: 125–31.Google Scholar
  98. Rehill BJ, Whitham TG, Martinsen GD, Schweitzer JA, Bailey JK, Lindroth RL. 2006. Developmental trajectories in cottonwood phytochemistry. J Chem Ecol 32: 2269–85.PubMedGoogle Scholar
  99. Rhodes DF, Cates RG. 1976. Toward a general theory of plant antiherbivores chemistry. Recent Advances Phytochemistry 10: 168–213.Google Scholar
  100. Robbins CT, Hanley TA., Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW. 1987. Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107.Google Scholar
  101. Scalbert A. 1991. Antimicrobial properties of tannins. Phytochemistry 30: 3875–83.Google Scholar
  102. 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 taiga floodplain soil: implications for changes in N cycling during succession. Can J Bot 74: 84–90.Google Scholar
  103. Schimel JP, Cates RG, Ruess R. 1998. The role of balsam poplar secondary chemicals in controlling soil nutrient dynamics through succession in the Alaskan taiga. Biogeochemistry 42: 221–34.Google Scholar
  104. Schultz JC. 1989. Tannin–insect interactions. In: Hemingway RW, Karchesy JJ, Eds. Chemistry and significance of condensed tannins. NY: Plenum Press. pp 416–33Google Scholar
  105. Schweitzer JA. 2002. Genetic variation associated with natural hybridization in Cottonwood affects riparian structure and function. Dissertation, Northern Arizona UniversityGoogle Scholar
  106. Schweitzer JA, Bailey JK, Rehill BJ, Hart SC, Lindroth RL, Keim P, Whitham TG. 2004. Genetically based trait in dominant tree affects ecosystem processes. Ecol Lett 7: 127–34.Google Scholar
  107. 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: 133–45.Google Scholar
  108. Schweitzer JA, Bailey JK, Bangert RK, Hart SC, Whitham TG. 2007. The role of plant genetic variation in determining above- and belowground microbial communities. In: Bailey MJ, Lilley AK, Timms-Wilson TM, Spencer-Phillips, Eds. Microbial ecology of aerial plant surfaces. Wallingford, UK: CABI PublishingGoogle Scholar
  109. Stevens ML, Lindroth RL. 2005. Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145: 298–306.PubMedGoogle Scholar
  110. Stout RJ. 1989. Effects of condensed tannins on leaf processing in mid-latitude and tropical streams: A theoretical approach. Canadian Journal of Fishery Aquatics 46: 1097–106.Google Scholar
  111. Swain T. 1979. Tannins and lignins. Rosenthal GA, Janzen DH, editors. Herbivores: their interactions with secondary plant metabolites. Academic Press, New York. Pp. 657–82.Google Scholar
  112. Treseder KL, Vitousek PM. 2001. Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawaii. Oecologia 126: 266–75.Google Scholar
  113. Tsai C-J, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y. 2006. Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172: 47–52.PubMedGoogle Scholar
  114. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, others. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313:1596–604Google Scholar
  115. Verkaik E, Jongkind A, Berendse F. 2006. Short-term and long-term effects of tannins on nitrogen mineralisation and litter decomposition in kauri (Agathis australis (D. Don) Lindl.) forests. Plant Soil 287: 337–45.Google Scholar
  116. Waltz AM, Whitham TG. 1997. Plant development affects arthropod communities: Opposing impacts of species removal. Ecology 78: 2133–44.CrossRefGoogle Scholar
  117. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GD, 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. Nature Reviews Genetics 7: 510–23.PubMedGoogle Scholar
  118. Whitham TG, DiFazio SP, Schweitzer JA, Shuster SM, Allan JG, Bailey JK, Woolbright SA. 2008. Extending genomics to natural communities and ecosystems. Science 320:492–5.PubMedGoogle Scholar
  119. Woolbright S. 2001. Genetic analyses of a synthetic population of hybrid cottonwoods with implications for community-level processes. Master’s thesis, Northern Arizona UniversityGoogle Scholar
  120. Wooley SC, Walker SC, Vernon J, Lindroth RL. 2008. Aspen decline, aspen chemistry, and elk herbivory: Are they linked? Rangelands 30:17–21.Google Scholar
  121. Xie D-Y, Sharma SB, Paiva NL, Ferreira D, Dixon RA. 2003. Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299: 396–9.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Jennifer A. Schweitzer
    • 1
  • Michael D. Madritch
    • 2
  • Joseph K. Bailey
    • 1
  • Carri J. LeRoy
    • 3
  • Dylan G. Fischer
    • 3
  • Brian J. Rehill
    • 4
  • Richard L. Lindroth
    • 2
  • Ann E. Hagerman
    • 5
  • Stuart C. Wooley
    • 6
  • Stephen C. Hart
    • 7
  • Thomas G. Whitham
    • 8
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  2. 2.Department of EntomologyUniversity of WisconsinMadisonUSA
  3. 3.Evergreen State CollegeOlympiaUSA
  4. 4.Department of ChemistryU.S. Naval AcademyAnnapolisUSA
  5. 5.Department of Chemistry and BiochemistryMiami UniversityOxfordUSA
  6. 6.Department of Biological SciencesCalifornia State UniversityTurlockUSA
  7. 7.School of Forestry and Merriam-Powell Center for Environmental ResearchNorthern Arizona UniversityFlagstaffUSA
  8. 8.Department of Biological Sciences and Merriam-Powell Center for Environmental ResearchNorthern Arizona UniversityFlagstaffUSA

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