Ecosystems

, Volume 18, Issue 7, pp 1269–1280 | Cite as

Environmental Filtering and Positive Plant Litter Feedback Simultaneously Explain Correlations Between Leaf Traits and Soil Fertility

  • Daniel C. Laughlin
  • Sarah J. Richardson
  • Elaine F. Wright
  • Peter J. Bellingham
Article

Abstract

Plant traits covary with soil fertility, but determining whether this is the outcome of environmental filtering or plant feedback is not straightforward, especially in long-lived plant communities such as rain forests. Without explicitly accounting for the potential of plant litter to influence soil properties, it is difficult to interpret with confidence that covariation between soil nutrients and plant traits is the outcome of environmental filtering. We estimated abundance-weighted mean leaf dry matter content (LDMC), senesced leaf litter nitrogen resorption proficiency (litter N %), wood tissue density, and multiple metrics of soil fertility (pH, C:N ratio, and organic P concentrations) on 241 temperate rain forest plots throughout New Zealand. A non-recursive structural equation model indicated that environmental filtering and plant litter feedback were equally important reciprocal processes that explain covariation between leaf traits and soil fertility. Plant communities with high resorption proficiency, high LDMC, and high stem tissue density were strongly associated with low-fertility soils. Both structural (LDMC) and chemical (litter N %) leaf traits influenced soil fertility, but stem tissue density did not exhibit feedback effects. Here, we show that it is not a matter of ‘either–or’ when determining the relative importance of environmental filtering and plant feedback, but rather that both processes are equally important and occur simultaneously in temperate forest ecosystems. Although both leaf and wood traits were filtered by soil fertility, only leaf traits exhibited significant feedback effects on soil fertility.

Keywords

leaf economic spectrum non-recursive model structural equation modeling plant–soil feedback nitrogen wood density 

Notes

Acknowledgements

This research was supported by a Grant (UOW1201) from the Royal Society of New Zealand Marsden Fund and Core funding for Crown Research Institutes from New Zealand’s Ministry of Business, Innovation and Employment’s Science and Innovation Group. This research uses publically available data of forest composition on permanent forest plots and we acknowledge the use of data drawn from the Natural Forest plot data collected between January 2002 and March 2007 by the LUCAS programme for the Ministry for the Environment. We thank Meredith McKay and others in the Department of Conservation for their contributions to data collection and management, and we thank the two anonymous reviewers, Peter Vitousek and Louis Schipper for their constructive comments and feedback. Data are available from the National Vegetation Survey databank (https://nvs.landcareresearch.co.nz/).

Supplementary material

10021_2015_9899_MOESM1_ESM.docx (151 kb)
Supplementary material 1 (DOCX 152 kb)

References

  1. Achat DL, Bakker MR, Zeller B, Pellerin S, Bienaimé S, Morel C. 2010. Long-term organic phosphorus mineralization in Spodosols under forests and its relation to carbon and nitrogen mineralization. Soil Biol Biochem 42:1479–90.CrossRefGoogle Scholar
  2. Aerts R, Chapin FSIII. 1999. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67.CrossRefGoogle Scholar
  3. Allen RB, Clinton PW, Davis MR. 1997. Cation storage and availability along a Nothofagus forest development sequence in New Zealand. Can J For Res 27:323–30.CrossRefGoogle Scholar
  4. Anderson TM, Hopcraft JGC, Eby S, Ritchie M, Grace JB, Olff H. 2010. Landscape-scale analyses suggest both nutrient and antipredator advantages to Serengeti herbivore hotspots. Ecology 91:1519–29.CrossRefPubMedGoogle Scholar
  5. Aponte C, García LV, Marañón T. 2013. Tree species effects on nutrient cycling and soil biota: a feedback mechanism favouring species coexistence. For Ecol Manage 309:36–46.CrossRefGoogle Scholar
  6. Augusto L, Ranger J, Binkley D, Rothe A. 2002. Impact of several common tree species of European temperate forests on soil fertility. Ann For Sci 59:233–53.CrossRefGoogle Scholar
  7. Baxendale C, Orwin KH, Poly F, Pommier T, Bardgett RD. 2014. Are plant–soil feedback responses explained by plant traits? New Phytol 204:408–23.CrossRefPubMedGoogle Scholar
  8. Baylis G. 1980. Mycorrhizas and the spread of beech. N Z J Ecol 3:151–3.Google Scholar
  9. Becknell JM, Powers JS. 2014. Stand age and soils as drivers of plant functional traits and aboveground biomass in secondary tropical dry forest. Can J For Res 44:604–13.CrossRefGoogle Scholar
  10. Bellingham P, Walker L, Wardle D. 2001. Differential facilitation by a nitrogen-fixing shrub during primary succession influences relative performance of canopy tree species. J Ecol 89:861–75.CrossRefGoogle Scholar
  11. Bellingham PJ, Morse CW, Buxton RP, Bonner KI, Mason NW, Wardle DA. 2013. Litterfall, nutrient concentrations and decomposability of litter in a New Zealand temperate montane rain forest. N Z J Ecol 37:162–71.Google Scholar
  12. Binkley D. 1995. The influence of tree species on forest soils: processes and patterns. Special Publication-Agronomy Society of New Zealand 1–34.Google Scholar
  13. Binkley D, Driscoll CT, Allen HL, Schoeneberger P, McAvoy D. 2011. Acidic deposition and forest soils: context and case studies of the southeastern United States: Springer Publishing Company, Incorporated.Google Scholar
  14. Binkley D, Fisher R. 2012. Ecology and management of forest soils. Chichester, West Sussex: Wiley.Google Scholar
  15. Binkley D, Giardina C. 1998. Why do tree species affect soils? The warp and woof of tree-soil interactions. Biogeochemistry 42:89–106.CrossRefGoogle Scholar
  16. Blakemore LC, Searle PL, Daly BK. 1987. Methods for chemical analysis of soils. Wellington: New Zealand Soil Bureau Scientific Report 80. DSIR.Google Scholar
  17. Bloomfield C. 1953. A study of podzolisation. Part II. The mobilization of iron and aluminium by the leaves and bark of Agathis australis (kauri). J Soil Sci 4:17–23.CrossRefGoogle Scholar
  18. Brinkman EP, Van der Putten WH, Bakker E-J, Verhoeven KJF. 2010. Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–73.CrossRefGoogle Scholar
  19. Buuren S, Groothuis-Oudshoorn K. 2011. MICE: multivariate imputation by chained equations in R. J Stat Softw 45:1–67.CrossRefGoogle Scholar
  20. Carvalho GH, Batalha MA, Silva IA, Cianciaruso MV, Petchey OL. 2014. Are fire, soil fertility and toxicity, water availability, plant functional diversity, and litter decomposition related in a Neotropical savanna? Oecologia 175:923–35.CrossRefPubMedGoogle Scholar
  21. Chapin FSIII, Vitousek PM, Cleve KV. 1986. The nature of nutrient limitation in plant communities. Am Nat 127:48–58.CrossRefGoogle Scholar
  22. Chapman SK, Langley JA, Hart SC, Koch GW. 2006. Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34.CrossRefPubMedGoogle Scholar
  23. Daniel MJ, Adams JA. 1984. Nutrient return by litterfall in evergreen podocarp-hardwood forest in New Zealand. NZ J Bot 22:271–83.CrossRefGoogle Scholar
  24. Davis MR, Allen RB, Clinton PW. 2004. The influence of N addition on nutrient content, leaf carbon isotope ratio, and productivity in a Nothofagus forest during stand development. Can J For Res 34:2037–48.CrossRefGoogle Scholar
  25. Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS. 2014. Mycorrhizas in changing ecosystems. Botany 92:149–60.CrossRefGoogle Scholar
  26. Ehrenfeld JG, Ravit B, Elgersma K. 2005. Feedback in the plant–soil system. Annu Rev Environ Resour 30:75–115.CrossRefGoogle Scholar
  27. Enright NJ. 1999. Litterfall dynamics in a mixed conifer-angiosperm forest in northern New Zealand. J Biogeogr 26:149–57.CrossRefGoogle Scholar
  28. Folmer EO, van der Geest M, Jansen E, Olff H, Anderson TM, Piersma T, van Gils JA. 2012. Seagrass–sediment feedback: an exploration using a non-recursive structural equation model. Ecosystems 15:1380–93.CrossRefGoogle Scholar
  29. Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu W, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao J, Cornelissen JHC. 2013. Linking litter decomposition of above- and below-ground organs to plant–soil feedbacks worldwide. J Ecol 101:943–52.CrossRefGoogle Scholar
  30. Frid A, Marliave J. 2010. Predatory fishes affect trophic cascades and apparent competition in temperate reefs. Biol Lett 6:533–6.PubMedCentralCrossRefPubMedGoogle Scholar
  31. Fujita Y, van Bodegom PM, Witte J-PM. 2013. Relationships between nutrient-related plant traits and combinations of soil N and P fertility measures. PLoS One 8:e83735.PubMedCentralCrossRefPubMedGoogle Scholar
  32. Gourlet-Fleury S, Rossi V, Rejou-Mechain M, Freycon V, Fayolle A, Saint-André L, Cornu G, Gérard J, Sarrailh J-M, Flores O, Baya F, Billand A, Fauvet N, Gally M, Henry M, Hubert D, Pasquier A, Picard N. 2011. Environmental filtering of dense-wooded species controls above-ground biomass stored in African moist forests. J Ecol 99:981–90.CrossRefGoogle Scholar
  33. Grace JB. 2006. Structural equation modeling and natural systems. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  34. Grace JB, Anderson TM, Smith MD, Seabloom E, Andelman SJ, Meche G, Weiher E, Allain LK, Jutila H, Sankaran M. 2007. Does species diversity limit productivity in natural grassland communities? Ecol Lett 10:680–9.CrossRefPubMedGoogle Scholar
  35. Grime JP. 1979. Plant strategies and vegetation processes. Chichester: Wiley.Google Scholar
  36. Grime JP. 1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–10.CrossRefGoogle Scholar
  37. Grubb PJ. 1998. A reassessment of the strategies of plants which cope with shortages of resources. Perspect Plant Ecol Evol Syst 1:3–31.CrossRefGoogle Scholar
  38. Heal O, Anderson J, Swift M. 1997. Plant litter quality and decomposition: an historical overview. In: Cadisch G, Giller KE, Eds. Driven by nature: plant litter quality and decomposition. Wallingford: CAB International. p 3–30.Google Scholar
  39. Hobbie SE. 1992. Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–9.CrossRefPubMedGoogle Scholar
  40. Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA. 2011. Species- and community-level patterns in fine root traits along a 120,000-year soil chronosequence in temperate rain forest. J Ecol 99:954–63.CrossRefGoogle Scholar
  41. Hook PB, Burke IC. 2000. Biogeochemistry in a shortgrass landscape: control by topography, soil texture, and microclimate. Ecology 81:2686–703.CrossRefGoogle Scholar
  42. Jager MM, Richardson SJ, Bellingham PJ, Clearwater MJ, Laughlin DC. 2015. Soil fertility induces coordinated responses of multiple independent functional traits. J Ecol 103:374–85.CrossRefGoogle Scholar
  43. Jenny H. 1941. Factors of soil formation: a system of quantitative pedology. New York: McGraw-Hill.Google Scholar
  44. Jongkind A, Velthorst E, Buurman P. 2007. Soil chemical properties under kauri (Agathis australis) in the Waitakere Ranges, New Zealand. Geoderma 141:320–31.CrossRefGoogle Scholar
  45. Keddy PA. 1992. Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–64.CrossRefGoogle Scholar
  46. Killingbeck KT. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–27.CrossRefGoogle Scholar
  47. Kline R. 2013. Reverse arrow dynamics. Formative measurement and feedback loops. In: Hancock GR, Mueller RO, Eds. Structural equation modeling: a second course. Greenwood: Information Age Publishing Inc. p 41–80.Google Scholar
  48. Kline RB. 2011. Principles and practice of structural equation modeling. New York: Guilford Press.Google Scholar
  49. Koele N, Dickie IA, Blum JD, Gleason JD, de Graaf L. 2014. Ecological significance of mineral weathering in ectomycorrhizal and arbuscular mycorrhizal ecosystems from a field-based comparison. Soil Biol Biochem 69:63–70.CrossRefGoogle Scholar
  50. Laughlin DC. 2011. Nitrification is linked to dominant leaf traits rather than functional diversity. J Ecol 99:1091–9.CrossRefGoogle Scholar
  51. Laughlin DC, Fulé PZ, Huffman DW, Crouse J, Laliberté E. 2011. Climatic constraints on trait-based forest assembly. J Ecol 99:1489–99.CrossRefGoogle Scholar
  52. Laughlin DC, Hart SC, Kaye JP, Moore MM. 2010a. Evidence for indirect effects of plant diversity and composition on net nitrification. Plant Soil 330:435–45.CrossRefGoogle Scholar
  53. Laughlin DC, Leppert JJ, Moore MM, Sieg CH. 2010b. A multi-trait test of the leaf-height-seed plant strategy scheme with 133 species from a pine forest flora. Funct Ecol 24:493–501.CrossRefGoogle Scholar
  54. Leathwick J, Wilson G, Rutledge D, Wardle P, Morgan F, Johnston K, McLeod M, Kirkpatrick R. 2003. Land environments of New Zealand. Auckland: David Bateman Ltd.Google Scholar
  55. Leathwick JR, Austin MP. 2001. Competitive interactions between tree species in New Zealand’s old-growth indigenous forests. Ecology 82:2560–73.CrossRefGoogle Scholar
  56. Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, Bodegom PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A. 2015. Global effects of soil and climate on leaf photosynthetic traits and rates. Global Ecol Biogeogr (in press).Google Scholar
  57. Mason NWH, Peltzer DA, Richardson SJ, Bellingham PJ, Allen RB. 2010. Stand development moderates effects of ungulate exclusion on foliar traits in the forests of New Zealand. J Ecol 98:1422–33.CrossRefGoogle Scholar
  58. McNab WH. 1993. A topographic index to quantify the effect of mesoscale landform on site productivity. Can J For Res 23:1100–7.CrossRefGoogle Scholar
  59. Metson AJ, Blakemore LC, Rhoades DA. 1979. Methods for the determination of soil organic carbon: a review, and application to New Zealand soils. N Z J Sci 22:205–28.Google Scholar
  60. Norris M, Avis P, Reich P, Hobbie S. 2013. Positive feedbacks between decomposition and soil nitrogen availability along fertility gradients. Plant Soil 367:347–61.CrossRefGoogle Scholar
  61. Ordoñez JC, Van Bodegom PM, Witte J-PM, Wright IJ, Reich PB, Aerts R. 2009. A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–49.CrossRefGoogle Scholar
  62. Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, Bardgett RD. 2010. Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–83.CrossRefGoogle Scholar
  63. Pakeman RJ, Quested HM. 2007. Sampling plant functional traits: what proportion of the species need to be measured? Appl Veg Sci 10:91–6.CrossRefGoogle Scholar
  64. 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 65:256–68.CrossRefGoogle Scholar
  65. Pastor J, Gardner R, Dale V, Post W. 1987. Successional changes in nitrogen availability as a potential factor contributing to spruce declines in boreal North America. Can J For Res 17:1394–400.CrossRefGoogle Scholar
  66. Peltzer DA, Allen RB, Bellingham PJ, Richardson SJ, Wright EF, Knightbridge PI, Mason NWH. 2014. Disentangling drivers of tree population size distributions. For Ecol Manage 331:165–79.CrossRefGoogle Scholar
  67. Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR. 2010. Understanding ecosystem retrogression. Ecol Monogr 80:509–29.CrossRefGoogle Scholar
  68. Poorter L, Wright SJ, Paz H, Ackerly DD, Condit R, Ibarra-Manríquez G, Harms KE, Licona JC, Martínez-Ramos M, Mazer SJ, Muller-Landau HC, Peña-Claros M, Webb CO, Wright IJ. 2008. Are functional traits good predictors of demographic rates? Evidence from five Neotropical forests. Ecology 89:1908–20.CrossRefPubMedGoogle Scholar
  69. Porder S, Vitousek PM, Chadwick OA, Chamberlain CP, Hilley GE. 2007. Uplift, erosion, and phosphorus limitation in terrestrial ecosystems. Ecosystems 10:159–71.CrossRefGoogle Scholar
  70. Quested H, Eriksson O, Fortunel C, Garnier E. 2007. Plant traits relate to whole-community litter quality and decomposition following land use change. Funct Ecol 21:1016–26.CrossRefGoogle Scholar
  71. Reich PB, Walters MB, Ellsworth DS. 1997. From tropics to tundra: Global convergence in plant functioning. Proc Natl Acad Sci 94:13730–4.PubMedCentralCrossRefPubMedGoogle Scholar
  72. Richardson SJ, Allen RB, Doherty JE. 2008. Shifts in leaf N: P ratio during resorption reflect soil P in temperate rainforest. Funct Ecol 22:738–45.CrossRefGoogle Scholar
  73. Rosseel Y. 2012. lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36.CrossRefGoogle Scholar
  74. Sayer EJ, Wright SJ, Tanner EV, Yavitt JB, Harms KE, Powers JS, Kaspari M, Garcia MN, Turner BL. 2012. Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15:387–400.CrossRefGoogle Scholar
  75. Scalbert A. 1992. Tannins in woods and their contribution to microbial decay prevention. In: Hemingway R, Laks P, Eds. Plant Polyphenols. Berlin: Springer. p 935–52.CrossRefGoogle Scholar
  76. 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 7:127–34.CrossRefGoogle Scholar
  77. Scott NA, Binkley D. 1997. Foliage litter quality and annual net N mineralization: comparison across North American forest sites. Oecologia 111:151–9.CrossRefGoogle Scholar
  78. Silver WL, Neff J, McGroddy M, Veldkamp E, Keller M, Cosme R. 2000. Effects of soil texture on belowground carbon and nutrient storage in a lowland Amazonian forest ecosystem. Ecosystems 3:193–209.CrossRefGoogle Scholar
  79. Silvester WB. 2000. The biology of kauri (Agathis australis) in New Zealand II. Nitrogen cycling in four kauri forest remnants. NZ J Bot 38:205–20.CrossRefGoogle Scholar
  80. Swenson NG, Weiser MD. 2010. Plant geography upon the basis of functional traits: an example from eastern North American trees. Ecology 91:2234–41.CrossRefPubMedGoogle Scholar
  81. Turner BL, Condron LM, Richardson SJ, Peltzer DA, Allison VJ. 2007. Soil organic phosphorus transformations during pedogenesis. Ecosystems 10:1166–81.CrossRefGoogle Scholar
  82. Turner I. 1994. Sclerophylly: primarily protective? Funct Ecol 8:669–75.CrossRefGoogle Scholar
  83. van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA. 2013. Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–76.CrossRefGoogle Scholar
  84. Vincent AG, Turner BL, Tanner EVJ. 2010. Soil organic phosphorus dynamics following perturbation of litter cycling in a tropical moist forest. Eur J Soil Sci 61:48–57.CrossRefGoogle Scholar
  85. Vitousek PM. 1982. Nutrient cycling and nutrient use efficiency. Am Nat 119:553–72.CrossRefGoogle Scholar
  86. Vitousek PM, Aplet G, Turner D, Lockwood JJ. 1992. The Mauna Loa environmental matrix: foliar and soil nutrients. Oecologia 89:372–82.CrossRefGoogle Scholar
  87. Vitousek PM, Turner DR, Kitayama K. 1995. Foliar nutrients during long-term soil development in Hawaiian montane rain forest. Ecology 76:712–20.CrossRefGoogle Scholar
  88. Wardle DA, Bellingham PJ, Kardol P, Giesler R, Tanner EVJ. 2015. Coordination of aboveground and belowground responses to local-scale soil fertility differences between two contrasting Jamaican rain forest types. Oikos 124:285–97.CrossRefGoogle Scholar
  89. Wardle DA, Wiser SK, Allen RB, Doherty JE, Bonner KI, Williamson WM. 2008. Aboveground and belowground effects of single-tree removals in New Zealand rain forest. Ecology 89:1232–45.CrossRefPubMedGoogle Scholar
  90. Wardle J. 1984. The New Zealand beeches: ecology, utilisation and management. Christchurch: N Z For Serv.Google Scholar
  91. Warton DI, Duursma RA, Falster DS, Taskinen S. 2012. smatr 3—an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–9.CrossRefGoogle Scholar
  92. Weiher E, Forbes S, Schauwecker T, Grace JB. 2004. Multivariate control of plant species richness and community biomass in blackland prairie. Oikos 106:151–7.CrossRefGoogle Scholar
  93. Werner FA, Homeier J. 2015. Is tropical montane forest heterogeneity promoted by a resource-driven feedback cycle? Evidence from nutrient relations, herbivory and litter decomposition along a topographical gradient. Funct Ecol 29:430–40.CrossRefGoogle Scholar
  94. Wong C-S, Law KS. 1999. Testing reciprocal relations by nonrecursive structural equation models using cross-sectional data. Organ Res Methods 2:69–87.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Daniel C. Laughlin
    • 1
  • Sarah J. Richardson
    • 2
  • Elaine F. Wright
    • 3
  • Peter J. Bellingham
    • 2
  1. 1.Environmental Research Institute and School of ScienceUniversity of WaikatoHamiltonNew Zealand
  2. 2.Landcare ResearchLincolnNew Zealand
  3. 3.Department of ConservationChristchurchNew Zealand

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