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Responses to predation risk cues and alarm pheromones affect plant virus transmission by an aphid vector

  • Behavioral ecology – original research
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Abstract

Herbivores assess predation risk in their environment by identifying visual, chemical, and tactile predator cues. Detection of predator cues can induce risk-avoidance behaviors in herbivores that affect feeding, dispersal, and host selection in ways that minimize mortality and reproductive costs. For herbivores that transmit plant pathogens, including many aphids, changes in herbivore behavior in response to predator cues may also affect pathogen spread. However, few studies have assessed how aphid behavioral responses to different types of predator cues affect pathogen transmission. Here, we conducted greenhouse experiments to assess whether responses of pea aphids (Acyrthosiphon pisum) to predation risk and alarm pheromone (E-β-Farnesene), an aphid alarm signal released in response to predation risk, affected transmission of Pea enation mosaic virus (PEMV). We exposed A. pisum individuals to risk cues, and quantified viral titer in aphids and pea (Pisum sativum) host plants across several time periods. We also assessed how A. pisum responses to risk cues affected aphid nutrition, reproduction, and host selection. We show that exposure to predator cues and alarm pheromone significantly reduced PEMV acquisition and inoculation. Although vectors avoided hosts with predator cues, predator cues did not alter vector reproduction or reduce nutrient acquisition. Overall, these results suggest that non-consumptive effects of predators may indirectly decrease the spread of plant pathogens by altering vector behavior in ways that reduce vector competence and pathogen transmission efficiency.

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Acknowledgements

This research was supported by USDA-NIFA Grant 2019-67011-29602 to BWL and USDA-NIFA Grant 2017-67013-26537 to DWC and CLC. We thank Crowder lab undergraduate assistants, Megan Asche for graphics creation, and D. Shorts and T. C. Koji for inspiration.

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Contributions

BWL, SB, and DWC conceived the experiments. BWL, SB, SB, and CLC performed the experiments. BWL analyzed the data. BWL and DWC wrote the manuscript. All authors provided editorial assistance.

Corresponding author

Correspondence to Benjamin W. Lee.

Additional information

Communicated by Sylvain Pincebourde.

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Supplementary file1 (DOCX 157 kb)

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Lee, B.W., Basu, S., Bera, S. et al. Responses to predation risk cues and alarm pheromones affect plant virus transmission by an aphid vector. Oecologia 196, 1005–1015 (2021). https://doi.org/10.1007/s00442-021-04989-6

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  • DOI: https://doi.org/10.1007/s00442-021-04989-6

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