The effect of predator presence on the behavioral sequence from host selection to reproduction in an invulnerable stage of insect prey
Predator–prey interactions primarily focus on prey life-stages that are consumed. However, animals in less vulnerable life-stages might also be influenced by the presence of a predator, making our understanding of predation-related impacts across all life-stages of prey essential. It has been previously demonstrated that Podisus maculiventris is a voracious predator of eggs and larvae of Leptinotarsa decemlineata, and that larvae will alter their behavior to avoid predation. However, the adult beetles are not readily consumed by P. maculiventris, raising the question of whether they will respond to predators to protect themselves or their offspring. Here, we examine the effect of predation risk by P. maculiventris, on three adult behaviors of L. decemlineata; colonization, oviposition, and feeding, and the resulting impact on host plant damage. In an open-field test, there was no difference in natural beetle colonization between plots with predation risk and control treatments. However, subsequent host plant damage by adult beetles was 63.9% less in predation risk treatments. Over the lifetime of adult beetles in field mesocosms, per capita feeding was 23% less in the predation risk treatment. Beetle oviposition was 37% less in the presence of predators in a short-term, greenhouse assay, and marginally reduced in longer term field mesocosms. Our results indicate that predation risk can drive relatively invulnerable adult herbivores to adjust behaviors that affect themselves (feeding) and their offspring (oviposition). Thus, the full impact of predator presence must be considered across the prey life cycle.
KeywordsNon-lethal effects Trait-mediated interactions Predation risk Non-consumptive effects Tri-trophic interactions Colorado potato beetle
We thank Marie Russel, Elizabeth Davidson-Lowe, Alyssa Cowles, Scott Nelson, Stephen Pecylak, Evan Hoki, and Dylan Beal for assistance in running experiments. Special thanks to Charlie Linn, Katja Poveda, Jared G. Ali, Douglas A. Landis, and two anonymous reviewers for thoughtful comments on the working manuscript. This project was supported by NIFA 2013-02649 and NYC-139851.
SH and JT formulated the study, performed the experiments, designed the experiments and wrote the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Boiteau G (1988) Sperm utilization and post-copulatory female-guarding in the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 47:183–187. https://doi.org/10.1111/j.1570-7458.1988.tb01134.x CrossRefGoogle Scholar
- Chamaillé-Jammes S, Malcuit H, Le Saout S, Martin J-L (2014) Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence. Oecologia 174:1151–1158. https://doi.org/10.1007/s00442-013-2843-0 CrossRefPubMedGoogle Scholar
- Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14. https://doi.org/10.1111/j.1570-7458.1988.tb02275.x CrossRefGoogle Scholar
- Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. https://doi.org/10.1890/0012-9658(2003)084[1083:Arotii]2.0.Co;2 CrossRefGoogle Scholar
- Wheeler D (2009) Suitability of different artificial diets for development and survival of stages of the predaceous ladybird. Annu Rev Entomol 41:10–12. https://doi.org/10.1146/annurev.en.41.010196.002203 Google Scholar