Ecosystems

, Volume 19, Issue 8, pp 1478–1490 | Cite as

Litter Chemistry, Community Shift, and Non-additive Effects Drive Litter Decomposition Changes Following Invasion by a Generalist Pathogen

Article

Abstract

Forest pathogens have strong potential to shape ecosystem function by altering litterfall, microclimate, and changing community structure. We quantified changes in litter decomposition from a set of distinct diseases caused by Phytophthora ramorum, an exotic generalist pathogen. Phytophthora ramorum causes leaf blight and increased litterfall %N, but no mortality on California bay laurel (Umbellularia californica), a common overstory tree that accumulates high levels of infection. Lethal twig and bole cankers on tanoak (Notholithocarpus densiflorus) lead to the disease sudden oak death which creates canopy openings and alters litterfall in mixed-species forests dominated by redwood (Sequoia sempervirens) which is minimally susceptible. Species identity had the greatest effect on mass loss and N dynamics with the most rapid rates in bay laurel, slowest in redwood, and intermediate in tanoak. Decomposing litter from infected sources had increased N accumulation, and although these changes were of lower magnitude relative to species identity, the region-scale invasion of P. ramorum suggests that this effect could occur over an extensive area. Canopy mortality was a significant and slowing influence on litter N dynamics in all species and also dampened non-additive effects within mixed litter bags. Redwood—the lowest quality litter—demonstrated non-additive interactions with consistently lower C:N when decomposed in mixed litter bags, but this effect did not alter the entire mixture. Mortality and subsequent changes in community composition have the greatest magnitude effects on litter decomposition for sudden oak death, but our study implies that different and sometimes cryptic mechanisms will drive decomposition changes for other forest diseases.

Keywords

Phytophthora ramorum sudden oak death tanoak California bay laurel tree mortality forest disease ecosystem function carbon nitrogen 

Notes

Acknowledgements

We thank H. Mehl and C. Shoemaker for their field and laboratory support of this research. We thank J. Ashander and S. Ibanez for feedback on the statistical analysis and Gary Lovett and two anonymous reviewers for helpful comments on earlier versions of this manuscript. We are grateful to the California State Parks and the Marin Municipal Water District for facilitating this research on their lands. This work was funded by NSF Grant DEB EF-0622770 as part of the joint NSF-NIH Ecology of Infectious Disease program, the Gordon and Betty Moore Foundation, and the USDA Forest Service Pacific Southwest Research Station.

Supplementary material

10021_2016_17_MOESM1_ESM.pdf (557 kb)
Supplementary material 1 (PDF 557 kb)

References

  1. Adair EC, Hobbie SE, Hobbie RK. 2010. Single-pool exponential decomposition models: potential pitfalls in their use in ecological studies. Ecology 91:1225–36.CrossRefPubMedGoogle Scholar
  2. Ball BA, Bradford MA, Hunter MD. 2008. Nitrogen and phosphorus release from mixed litter layers is lower than predicted from single species decay. Ecosystems 12:87–100.CrossRefGoogle Scholar
  3. Berglund SL, Ågren GI, Ekblad A. 2013. Carbon and nitrogen transfer in leaf litter mixtures. Soil Biol Biochem 57:341–8.CrossRefGoogle Scholar
  4. Chapman SK, Hart SC, Cobb NS, Whitham TG, Koch GW. 2003. Insect herbivory increases litter quality and decomposition: an extension of the acceleration hypothesis. Ecology 84:2867–76.CrossRefGoogle Scholar
  5. Chapman SK, Newman GS, Hart SC, Schweitzer JA, Koch GW. 2013. Leaf litter mixtures alter microbial community development: mechanisms for non-additive effects in litter decomposition. PLoS ONE 8:e62671.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Classen AT, Hart SC, Whitman TG, Cobb NS, Koch GW. 2005. Insect infestations linked to shifts in microclimate. Soil Sci Soc Am J 69:2049–57.CrossRefGoogle Scholar
  7. Cobb RC. 2010. Species shift drives decomposition rates following invasion by hemlock woolly adelgid. Oikos 119:1291–8.CrossRefGoogle Scholar
  8. Cobb RC, Eviner VT, Rizzo DM. 2013. Mortality and community changes drive sudden oak death impacts on litterfall and soil nitrogen cycling. New Phytol 200:422–31.CrossRefPubMedGoogle Scholar
  9. Cobb RC, Filipe JAN, Meentemeyer RK, Gilligan CA, Rizzo DM. 2012. Ecosystem transformation by emerging infectious disease: loss of large tanoak from California forests. J Ecol 100:712–22.CrossRefGoogle Scholar
  10. Cobb RC, Meentemeyer RK, Rizzo DM. 2010. Apparent competition in canopy trees determined by pathogen transmission rather than susceptibility. Ecology 91:327–33.CrossRefPubMedGoogle Scholar
  11. Cobb RC, Orwig DA, Currie S. 2006. Decomposition of green foliage in eastern hemlock forests of southern New England impacted by hemlock woolly adelgid infestations. Can J For Res 36:1331–41.CrossRefGoogle Scholar
  12. Davidson JM, Patterson HA, Rizzo DM. 2008. Sources of inoculum for Phytophthora ramorum in a redwood forest. Phytopathology 98:860–6.CrossRefPubMedGoogle Scholar
  13. Davidson JM, Patterson HA, Wickland AC, Fichtner EJ, Rizzo DM. 2011. Forest type influences transmission of Phytophthora ramorum in California oak woodlands. Phytopathology 101:492–501.CrossRefPubMedGoogle Scholar
  14. Davidson JM, Wickland AC, Patterson HA, Falk KR, Rizzo DM. 2005. Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology 95:587–96.CrossRefPubMedGoogle Scholar
  15. Desprez-Loustau M-L, Robin C, Buée M, Courtecuisse R, Garbaye J, Suffert F, Sache I, Rizzo DM. 2007. The fungal dimension of biological invasions. Trends Ecol Evol 22:472–80.CrossRefPubMedGoogle Scholar
  16. DiLeo MV, Bostock RM, Rizzo DM. 2009. Phytophthora ramorum does not cause physiologically significant systemic injury to California bay laurel, its primary reservoir host. Phytopathology 99:1307–11.CrossRefPubMedGoogle Scholar
  17. Edburg SL, Hicke JA, Brooks PD, Pendall EG, Ewers BE, Norton U, Gochis D, Gutmann ED, Meddens AJ. 2012. Cascading impacts of bark beetle-caused tree mortality on coupled biogeophysical and biogeochemical processes. Front Ecol Environ 10:416–24.CrossRefGoogle Scholar
  18. Eviner VT, Likens GE. 2008. Effects of pathogens on terrestrial ecosystem function. In: Ostfeld RS, Keesing F, Eviner VT, Eds. Infectious disease ecology. Effects of ecosystems on disease and disease on ecosystems. Princeton: Princeton University Press. p 260–83.Google Scholar
  19. Gandhi KJK, Herms DA. 2010. Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405.CrossRefGoogle Scholar
  20. Garbelotto M, Hayden KJ. 2012. Sudden Oak death: interactions of the exotic oomycete Phytophthora ramorum with naïve North American hosts. Eukaryot Cell 11:1313–23.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hansen EM. 1999. Disease and diversity in forest ecosystems. Australas Plant Pathol 28:313–19.CrossRefGoogle Scholar
  22. Hansen EM, Reeser PW, Sutton W. 2012. Phytophthora beyond agriculture. Annu Rev Phytopathol 50:359–78.CrossRefPubMedGoogle Scholar
  23. Harrington TB, Tappeiner JC. 2009. Long-term effects of tanoak competition on Douglas-fir stand development. Can J For Res 39:765–76.CrossRefGoogle Scholar
  24. Hart SC, Firestone MK, Paul EA. 1992. Decomposition and nutrient dynamics of ponderosa pine needles in a Mediterranean-type climate. Can J For Res 22:306–14.CrossRefGoogle Scholar
  25. Hicke JA, Allen CD, Desai AR, Dietze MC, Hall RJ, Hogg EH, Kashian DM, Moore D, Raffa KF, Sturrock RN. 2012. Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Glob Change Biol 18:7–34.CrossRefGoogle Scholar
  26. Holt RD, Dobson AP, Begon M, Bowers RG, Schauber EM. 2003. Parasite establishment in host communities. Ecol Lett 6:837–42.CrossRefGoogle Scholar
  27. Hunter MD. 2002. Insect population dynamics meets ecosystem ecology: effects of herbivory on soil nutrient dynamics. Agric For Entomol 3:77–84.CrossRefGoogle Scholar
  28. Kuljian H, Varner JM. 2010. The effects of sudden oak death on foliar moisture content and crown fire potential in tanoak. For Ecol Manage 259:2103–10.CrossRefGoogle Scholar
  29. Lovett GM, Arthur MA, Weathers KC, Griffin JM. 2010. Long-term changes in forest carbon and nitrogen cycling caused by an introduced pest/pathogen complex. Ecosystems 13:1188–200.CrossRefGoogle Scholar
  30. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD. 2006. Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405.CrossRefGoogle Scholar
  31. Lummer D, Scheu S, Butenschoen O. 2012. Connecting litter quality, microbial community and nitrogen transfer mechanisms in decomposing litter mixtures. Oikos 121:1649–55.CrossRefGoogle Scholar
  32. Metz MR, Frangioso KM, Wickland AC, Meentemeyer RK, Rizzo DM. 2012. An emergent disease causes directional changes in forest species composition in coastal California. Ecosphere 3:art86.CrossRefGoogle Scholar
  33. Orwig DA, Cobb RC, D’Amato AW, Kizlinski ML, Foster DR. 2008. Multi-year ecosystem response to hemlock woolly adelgid infestation in southern New England forests. Can J For Res 38:834–43.CrossRefGoogle Scholar
  34. Orwig DA, Thompson JR, Povak NA, Manner M, Niebyl D, Foster DR. 2012. A foundation tree at the precipice: Tsuga canadensis health after the arrival of Adelges tsugae in central New England. Ecosphere 3:art10.CrossRefGoogle Scholar
  35. Ostry ME, Laflamme G. 2008. Fungi and diseases: natural components of healthy forests. Botany 87:22–5.CrossRefGoogle Scholar
  36. Preston DL, Mischler JA, Townsend AR, Johnson PTJ. 2016. Disease ecology meets ecosystem science. Ecosystems 19:737–48.CrossRefGoogle Scholar
  37. Quested HM, Callaghan TV, Cornelissen JHC, Press MC. 2005. The impact of hemiparasitic plant litter on decomposition: direct, seasonal and litter mixing effects. J Ecol 93:87–98.CrossRefGoogle Scholar
  38. Ramage BS, O’Hara KL, Forrestel AB. 2011. Forest transformation resulting from an exotic pathogen: regeneration and tanoak mortality in coast redwood stands affected by sudden oak death. Can J For Res 41:763–72.CrossRefGoogle Scholar
  39. Rizzo DM, Garbelotto M, Hansen EM. 2005. Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43:309–35.CrossRefPubMedGoogle Scholar
  40. Rizzo DM, Slaughter GW, Parmeter JR Jr. 2000. Enlargement of canopy gaps associated with a fungal pathogen in Yosemite Valley, California. Can J For Res 30:1501–10.CrossRefGoogle Scholar
  41. Rubino L, Charles S, Sirulnik AG, Tuininga AR, Lewis JD. 2015. Invasive insect effects on nitrogen cycling and host physiology are not tightly linked. Tree Physiol 35:124–33.CrossRefPubMedGoogle Scholar
  42. Ruess RW, McFarland JM, Trummer LM, Rohrs-Richey JK. 2009. Disease-mediated declines in N-fixation inputs by Alnus tenuifolia to early-successional floodplains in interior and south-central Alaska. Ecosystems 12:489–502.CrossRefGoogle Scholar
  43. Schweitzer JA, Bailey JK, Hart SC, Whitham TG. 2005. Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–40.CrossRefGoogle Scholar
  44. Shearer BL, Crane CE, Barrett S, Cochrane A. 2007. Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Aust J Bot 55:225–38.CrossRefGoogle Scholar
  45. Wickland AC, Jensen CE, Rizzo DM. 2008. Geographic distribution, disease symptoms and pathogenicity of Phytophthora nemorosa and Phytophthora pseudosyringae in California, USA. Forest Pathol 38:288–98.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Plant PathologyUniversity of CaliforniaDavisUSA

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