Abstract
The effects of experimental nitrogen (N) additions (0, 12.5, and 50 kg N ha−1 y−1) on long-term (12 years) understorey vegetation dynamics were examined in a boreal forest. The results showed that two types of natural enemies of the dominant dwarf-shrub Vaccinium myrtillus (pathogenic fungus of the species Valdensia heterodoxa and herbivorous larvae of the genus Operophtera) influenced the vegetation dynamics. The pathogenic fungus, causing premature leaf-shed of V. myrtillus, showed a strong positive N response during the initial 5-year period. For the larvae, a relatively modest N response was overshadowed by an almost 40-fold population increase during an outbreak event that followed the initial 5-year period. This outbreak occurred irrespective of N addition, resulting in V. myrtillus decline and depriving the pathogenic fungus of its substrate. Hence our study demonstrates that vegetation dynamics in this relatively species poor and seemingly simple ecosystem are driven by complex biotic interactions. Further, we show that an important component of these interactions is the temporal alternation of the two natural enemies and, resultant regulation of the dominant plant’s abundance. Finally, we emphasize that long-term data are essential to capture the complexity of this type of biotic interactions. In our case, a short-term study may have resulted in markedly different conclusions regarding effects of N enrichment and the role of biotic interactions for forest vegetation dynamics.
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References
Britton AJ, Fisher JM. 2007. Interactive effects of nitrogen deposition, fire and grazing on diversity and composition of low-alpine prostrate Calluna vulgaris heathland. J Appl Ecol 44:125–35.
Brunstig AMH, Heil GW. 1985. The role of nutrients in the interactions between a herbivorous beetle and some competing plant species in heathlands. Oikos 44:23–6.
Burdon JJ, Thrall PH, Ericson L. 2006. The current and future dynamics of disease in plant communities. Annu Rev Phytopathol 44:19–39.
Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D. 1997. Biotic control over the functioning of ecosystems. Science 277:500–4.
Forkner RE, Hunter MD. 2000. What goes up must come down? Nutrient additions and predation pressure on oak herbivores. Ecology 81:1588–600.
Gilliam FS. 2006. Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–91.
Hart SA, Chen YH. 2006. Understorey vegetation dynamics of North American boreal forests. Crit Rev Plant Sci 25:381–97.
Hawkins BA, Cornell HV, Hochberg ME. 1997. Predators, parasitoids and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–52.
Kerslake JE, Kruuk LEB, Hartley SE, Woodin SJ. 1996. Winter moth (Operophtera brumata (Lepidoptera: Geometridae)) outbreaks on Scottish heather moorlands: effects of host plant and parasitoids on larval survival and development. Bull Entomol Res 86:155–64.
Kytö M, Niemelä P, Larsson S. 1996. Insects on trees: population and individual response to fertilization. Oikos 75:148–59.
Lawton JG, Strong DR. 1981. Community patterns and folivorous insects. Am Nat 118:317–38.
Lepš J, Šmilauer P. 2003. Multivariate analysis of ecological data using CANOCO. Cambridge, UK: University Press. p 269.
Mattson WJ. 1980. Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–61.
Mitchell CE. 2003. Trophic control of grassland production and biomass by pathogens. Ecol Lett 6:147–55.
Nilsson MC, Wardle DA, Zackrisson O, Jäderlund A. 2002. Effects of alleviation of ecological stresses on an alpine tundra community over an 8-year period. Oikos 97:3–17.
Nordin A, Strengbom J, Witzell J, Näsholm T, Ericson L. 2005. Nitrogen deposition and the biodiversity of boreal forests—implications for the nitrogen critical load. Ambio 34:20–4.
Preisser EL, Strong DR. 2004. Climate affects predator control of an herbivore outbreak. Am Nat 163:754–62.
Raymond B, Vanbergen A, Watt A, Hartley SE, Cory JS, Hails RS. 2002. Escape from pupal predation as potential cause of outbreaks of the winter moth, Operophtera brumata. Oikos 98:219–28.
Ritchie ME. 2000. Nitrogen limitation and trophic versus abiotic influences on insect herbivores in a temperate grassland. Ecology 8:1601–12.
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH. 2000. Global biodiversity scenarios for the year 2100. Science 287:1770–4.
Strengbom J, Nordin A, Näsholm T, Ericson L. 2001. Slow recovery of boreal forest ecosystem following decreased nitrogen input. Funct Ecol 15:451–7.
Strengbom J, Nordin A, Näsholm T, Ericson L. 2002. Parasitic fungus mediates vegetation change in nitrogen exposed boreal forest. J Ecol 90:61–7.
Strengbom J, Witzell J, Nordin A, Ericson L. 2005. Do multitrophic interactions override N fertilization effects on Operophtera larvae? Oecologia 143:241–50.
Strengbom J, Englund G, Ericson L. 2006. Experimental scale and precipitation modify effects of nitrogen addition on a plant pathogen. J Ecol 94:227–33.
Vogelgsang S, Shamoun SF. 2002. Growth, sporulation, and conidia discharge of Valdensinia heterodoxa, a foliar pathogen of salal, as influenced by temperature and photoperiod in vitro. Mycol Res 106:480–90.
White TCR. 1993. The inadequate environment: nitrogen and the abundance of animals. Berlin, Germany: Springer. p 425.
Wiedermann MM, Nordin A, Gunnarsson U, Nilsson M, Ericson L. 2007. Global change shifts vegetation and plant–parasite interactions in a boreal mire. Ecology 88:454–64.
Zar JH. 1996. Biostatistical analysis. 3rd edn. New Jersey: Prentice-Hall. p 662.
Acknowledgments
We are grateful to Ann Sehlstedt for help in monitoring the vegetation, and the staff at the Svartberget field station for assistance during fertilizer applications. The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS), the Swedish Clean Air Program (SCARP) (supported by the Swedish Environmental Protection Board), and the Umeå Centre for Environmental Research (CMF) financially supported the project (all funding received by A. Nordin and L. Ericson).
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L. Ericson, A. Nordin, and J. Strengbom started the experiment. A. Nordin and J. Strengbom analyzed the data and outlined the content of the manuscript. All authors contributed to field-work and manuscript writing.
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Nordin, A., Strengbom, J., Forsum, Å. et al. Complex Biotic Interactions Drive Long-Term Vegetation Change in a Nitrogen Enriched Boreal Forest. Ecosystems 12, 1204–1211 (2009). https://doi.org/10.1007/s10021-009-9287-8
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DOI: https://doi.org/10.1007/s10021-009-9287-8