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Belowground fungal associations and water interact to influence the compensatory response of Ipomopsis aggregata

Abstract

Although the concept that some plants benefit from being eaten is counterintuitive, there is now considerable evidence demonstrating enhanced fitness following herbivory. It has been assumed that plants growing in high resource conditions are the ones best able to compensate for herbivory. However, just the opposite has been found for dicotyledonous plants exhibiting patterns of overcompensation, with most occurring in resource-poor conditions. Long-term studies of the monocarpic biennial, scarlet gilia, Ipomopsis aggregata growing in resource-poor conditions have shown that ungulate herbivory by mule deer and elk can result in a threefold increase in plant fitness over uneaten controls. These observations led us to hypothesize that fungal associations would facilitate the compensatory response most commonly observed in this Arizona population of scarlet gilia; perhaps mutualistic associations with fungi, such as arbuscular mycorrhizal fungi, would explain the phenomenon of overcompensation altogether. Fungal removal experiments, using Captan®, a commercially available fungicide, showed that a reduction in fungal abundance altered the compensatory response following ungulate herbivory, particularly in years in which water was limited, increasing fitness compensation from equal compensation to overcompensation. A multifactorial experiment revealed that the interactive effects of water and fungicide maximized fruit production following herbivory. Our results are counter to the “modification of tolerance hypothesis” in which plants associating with mycorrhizal fungi will have higher tolerance to herbivory. It is likely that arbuscular mycorrhizal fungi and dark septate endophytes compete with plants for photosynthates following herbivory, thereby limiting the magnitude of compensation. Thus, fungi appear to be parasitic on scarlet gilia following ungulate herbivory.

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Acknowledgments

We thank Drs. Carol Augspurger, Andrew Miller, Victoria Borowicz, Sara Paver, Katie Amato, Emily Wheeler-Lankau, Arianne Peralta, and Greg Spyreas for comments on the manuscript. A special thanks to Dr. Rick Lankau for statistical guidance along with detailed comments on the manuscript. Funding was provided by summer research fellowships awarded to C. M. Allsup through the Program for Ecology, Evolution, and Conservation Biology at the University of Illinois and NSF Grants 0092554 and 1146085 to K.N. Paige. In addition we wish to thank Brett Olds, Eric Scott, Denise Paige, Kelly Allsup, and Karlton Allsup for their help in the field.

Author contributions statement

CMA and KNP conceived and designed the experiments. CMA and KNP conducted the field work. CMA collected and analyzed the data. CMA and KNP wrote the manuscript.

Author information

Correspondence to Ken N. Paige.

Additional information

Communicated by Joel Sachs.

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Allsup, C.M., Paige, K.N. Belowground fungal associations and water interact to influence the compensatory response of Ipomopsis aggregata . Oecologia 180, 463–474 (2016). https://doi.org/10.1007/s00442-015-3470-8

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Keywords

  • Overcompensation
  • Ungulate herbivory
  • Fungi
  • Scarlet gilia