Neighborhood diversity simultaneously increased and decreased susceptibility to contrasting herbivores in an early stage forest diversity experiment

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Abstract

Forest structure and diversity can regulate tree vulnerability to damage by insects and pathogens. Past work suggests that trees with diverse neighbours should experience less leaf herbivory and less damage from specialist herbivores and diseases, and that the effect of neighbourhood diversity should be strongest at small spatial scales. In an early stage temperate tree diversity experiment, we monitored damage from leaf removing herbivores, specialist (gallers and leaf miners) herbivores, and two specialist fungal diseases (maple leaf anthracnose and cedar apple gall rust) over 3 years. The experimental design included treatments that varied independently in phylogenetic and functional diversity and we made our analyses across four spatial scales (1–16 m2). Neighborhood diversity simultaneously increased leaf removal for some species, decreased it for others, and had no effect on yet others. Height apparency—the difference between a focal plant’s height and its neighbours’—was the best single predictor of leaf removal across species and spatial scales, but the strength and direction of its effect were also species-specific. Specialist pathogens and fungal foliar diseases showed signs of associational resistance and susceptibility. Oaks (Quercus spp.) were more resistant to leaf miners and maples were more resistant to anthracnose when surrounded by diverse neighbours (associational resistance). In contrast, birches (Betula papyrifera) were more susceptible to leaf miners and eastern red cedars (Juniperus virginiana) were more susceptible to cedar apple gall rust (Gymnosporangium juniperi-virginianae) infection in diverse environments (associational susceptibility). Herbivore and pathogen damage was better predicted by community structure and diversity at small spatial scales (1 and 4 m2) than large scales (9 and 16 m2), suggesting a characteristic spatial scale for these biodiversity-ecosystem functioning effects. Synthesis. Humans control forest diversity through selective harvesting and planting in natural stands and plantations. Our experimental demonstration of the role of local community structure and diversity in suppressing some forms of pest and pathogen damage to trees suggests that forest management can be most effective when diversity is considered at small spatial scales and the underlying biology of particular pests, pathogens, and hosts is taken into account. Pictured here: the “galls” formed by cedar apple gall rust (Gymnosporangium juniperae-virginiae) on eastern red cedar (Juniperus virginiana) in early spring release wind-dispersed teleospores. Junipers showed associational susceptibility: greater susceptibility to gall rust with more diverse neighbours.

Original languageEnglish (US)
Pages (from-to)1492-1505
Number of pages14
JournalJournal of Ecology
Volume107
Issue number3
DOIs
StatePublished - May 2019

Bibliographical note

Funding Information:
This work was supported by grants from the US National Science Foundation Long-Term Ecological Research Program (LTER) including DEB-0620652 and DEB-1234162. Further support was provided by the Cedar Creek Ecosystem Science Reserve and the University of Minnesota. J.J.G. was supported by fellowships from the Crosby, Rothman, Wilkie, Anderson, and Dayton Funds; the Doctoral Dissertation Fellowship; and the department of Ecology, Evolution, and Behavior, all at the University of Minnesota, and by a visiting fellowship at the Arnold Arboretum of Harvard University. R.A.M. was supported by Minnesota Agriculture Experiment Station: MIN-42-060. The authors wish to thank Forest Isbell for providing statistical consulting and Allen J. Butterfield for making SLA and water content measurements. Rick Lindroth, Robert Blanchette, and Eric Lind provided helpful feedback on study design. Chris Buyarski, Troy Mielke, and many Cedar Creek interns played an essential role in establishing and maintaining the FAB experiment. Journal editors and anonymous reviewers provided helpful feedback, dramatically improving the ultimate manuscript.

Publisher Copyright:
© 2018 The Authors. Journal of Ecology © 2018 British Ecological Society

Keywords

  • anthracnose
  • cedar apple gall rust
  • ecological scale
  • gall
  • leaf miner
  • plant apparency
  • plant–herbivore interactions
  • resource concentration

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