Direct and Interactive Effects of Enemies and Mutualists on Plant Performance: A Meta-Analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant–enemy and plant–mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies

Appendix B. Host plant, pathogen, and AM fungus species included in chi-squared tests of plant, pathogen, and AM fungus growth and list of data sources.

Host plant, pathogen, and AM fungus species included in chi-squared tests of plant, pathogen, and AM fungus growth and list of data sources

Appendix A. Host plant, pathogen, and AM fungus species included in meta-analyses of plant, pathogen, and AM fungus growth and list of data sources.

Host plant, pathogen, and AM fungus species included in meta-analyses of plant, pathogen, and AM fungus growth and list of data sources

Direct and interactive effects of enemies and mutualists on plant performance: A meta-analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant–enemy and plant–mutualist interactions. We performed a meta?analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta?analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single?species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non?crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies.This work was conducted as part of the Biotic Interactions Working Group supported by the National Center for Ecological Analysis and Synthesis, a Center funded by NSF (Grant #DEB?0072909), the University of California, and the Santa Barbara campus

Appendix A. Articles and data used in the meta-analysis.

Articles and data used in the meta-analysis

Appendix B. Effect sizes and their sampling variances.

Effect sizes and their sampling variances

Appendix E. Results from subsampling studies from the entire data set.

Results from subsampling studies from the entire data set

Appendix C. Effect sizes using Hedges' d.

Effect sizes using Hedges' d

Appendix D. Effect sizes using different measures of plant performance.

Effect sizes using different measures of plant performance

Supplement 1. Information on studies used in the meta-analysis.

<h2>File List</h2><blockquote> <p><a href="MorrisEtAl_supplement.csv">MorrisEtAl_supplement.csv</a></p> </blockquote><h2>Description</h2><blockquote> <p>MorrisEtAl_supplement.csv is a comma-delimited text file that shows all of the unique agent pairs (e.g., the "Different Agents" column of <a href="appendix-A.htm">Appendix A</a>) and provides additional detailed information on all of the studies used in the meta-analysis.</p> <p>The following table describes the variables in the file:</p> -- TABLE: Please see in attached file. -- <p>Here are several additional notes relating to data collection.</p> <p>Plant performance measures included measures of size and measures of sexual reproduction. Only four studies included both types of measure. In those cases, for mainly clonally reproducing plants, we chose the measure of size, and otherwise used the sexual reproduction measure. When multiple measures of the same type (either size or reproduction) were presented in a study, we chose the one that best represented plant performance (e.g., total biomass over belowground biomass). We recovered numerical data from graphics using the program ImageJ:</p> <p>Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image Processing with ImageJ. Biophotonics International 11:36–42.</p> </blockquote