Multitrophic interactions mediate the effects of climate change on herbivore abundance

Abstract

Climate change can influence the abundance of insect herbivores through direct and indirect mechanisms. In this study, we evaluated multitrophic drivers of herbivore abundance for an aphid species (Aphis helianthi) in a subalpine food web consisting of a host plant (Ligusticum porteri), mutualist ants and predatory lygus bugs (Lygus spp.). We used a model-selection approach to determine which climate and host plant cues best predict year-to-year variation in insect phenology and abundance observed over 6 years. We complemented this observational study with experiments that determined how elevated temperature interacts with (1) host plant phenology and (2) the ant-aphid mutualism to determine aphid abundance. We found date of snowmelt to be the best predictor of yearly abundance of aphid and lygus bug abundance but the direction of this effect differed. Aphids achieved lower abundances in early snowmelt years likely due to increased abundance of lygus bug predators in these years. Elevating temperature of L. porteri flowering stalks reduced their quality as hosts for aphid populations. However, warming aphid colonies on host plants of similar quality increased population growth rates. Importantly, this effect was apparent even in the absence of ants. While we observed fewer ants tending colonies at elevated temperatures, these colonies also had reduced numbers of lygus bug predators. This suggests that mutualism with ants becomes less significant as temperature increases, which contrasts other ant-hemipteran systems. Our observational and experimental results show the importance of multitrophic species interactions for predicting the effect of climate change on the abundances of herbivores.

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Acknowledgements

A Research and Creative Work grant to EM through the University of Colorado Colorado Springs supported this research. The National Science Foundation grants DEB-9408382, IBN-9814509, DEB-0238331, DEB-0922080, and DEB-1354104 provided funding to DI for the plant phenology and abundance observations. We also thank the Rocky Mountain Biological Laboratory for hosting and permitting this research. Fieldwork included help from Gretchen Kraeger, Cheryl Sandrow and Brittany Smith.

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Authors

Contributions

EM, DI and JO designed and performed the observational study. AR and EM conceived and designed the manipulative experiments. EM and AR performed the manipulative experiments. AR and EM analyzed the data. AR wrote the original version of the manuscript, and EM and DI revised and edited the final submitted version.

Corresponding author

Correspondence to Emily H. Mooney.

Additional information

Communicated by Amy Austin.

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Robinson, A., Inouye, D.W., Ogilvie, J.E. et al. Multitrophic interactions mediate the effects of climate change on herbivore abundance. Oecologia 185, 181–190 (2017). https://doi.org/10.1007/s00442-017-3934-0

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Keywords

  • Herbivory
  • Ant-aphid mutualism
  • Phenology
  • Warming experiment