Herbivore density mediates the indirect effect of herbivores on plants via induced resistance and apparent competition

Ricardo A Ramirez,Micky D Eubanks

doi:10.1002/ecs2.1218

Abstract

AbstractHerbivore‐induced plant resistance and apparent competition are two indirect ways herbivores interact. If a less damaging herbivore indirectly suppresses the abundance of a more damaging herbivore via these mechanisms, then plants may ultimately benefit. Changes in herbivore density, however, can dictate the intensity of species interactions and may play a critical role in determining the outcome of plant‐ and predator‐mediated herbivore interactions. We tested the effects of herbivore density on the strength of indirect interactions among phloem‐feeding aphids and herbivorous caterpillars and the outcome of these interactions for their shared host plant, cotton (Gossypium hirsutum). We quantified the survival of caterpillars on host plants that were infested with varying densities of aphids in the presence and absence of predators (ladybeetles). We found that aphids induced defensive proteins in cotton plants and that caterpillar survival was negatively affected by induced resistance. Likewise, we found that the presence of aphids increased predation of caterpillars by ladybeetles, but that apparent competition between aphids and caterpillars was density dependent. Ladybeetles consumed relatively high numbers of small caterpillars at low to intermediate aphid densities, but essentially became aphid specialists at high aphid densities. Aphid induced defenses and apparent competition combined such that plant damage by caterpillars was lowest when predators were present at low aphid density (induced resistance + highest level of apparent competition). This suggests that herbivores can benefit plants, but the effect on host plants is mediated by herbivore density. Indirect herbivore‐plant mutualisms may increase plant quality, plant fitness, and yield of crop plants and these interactions need to be considered in ecologically based pest management plans. In addition, these interactions likely alter arthropod community structure and natural selection on anti‐herbivore defense traits in plants in natural systems.

Highlights

Insect herbivores frequently interact indirectly through interactions mediated by both plant and predators (Strauss 1991, Denno et al 1995, Stachowicz 2001, Kaplan and Denno 2007, Eubanks and Finke 2014)
We found a significant aphid density × predator interaction on caterpillar survival in the field (F2,33 = 5.01, P = 0.013) (Fig. 2)
Our data suggest that it is possible for aphids to benefit plants by reducing caterpillar survival, this effect was dependent on aphid density

Summary

Introduction

Insect herbivores frequently interact indirectly through interactions mediated by both plant and predators (Strauss 1991, Denno et al 1995, Stachowicz 2001, Kaplan and Denno 2007, Eubanks and Finke 2014). RAMIREZ AND EUBANKS (apparent competition sensu lato) (Holt 1977) In both cases, an herbivore may provide a net benefit to the plant they consume if that herbivore indirectly suppresses the abundance of a more damaging herbivore (e.g., Halitschke et al 2011, Eubanks and Finke 2014). Induced plant resistance through changes in plant quality can reduce herbivore feeding, development and performance (Ryan 1990, Felton et al 1992, Lawrence and Novak 2006). These interactions become more complex when multiple herbivore species are involved. An overwhelming number of studies, show that feeding from one herbivore species can negatively impact a subsequent herbivore species through these plant-mediated effects (see examples in Kaplan and Denno 2007)

Methods

Results

Conclusion