Habitat preference of an herbivore shapes the habitat distribution of its host plant

Abstract

Plant distributions can be limited by habitat-biased herbivory, but the proximate causes of such biases are rarely known. Distinguishing plant-centric from herbivore-centric mechanisms driving differential herbivory between habitats is difficult without experimental manipulation of both plants and herbivores. Here we tested alternative hypotheses driving habitat-biased herbivory in bittercress (Cardamine cordifolia), which is more abundant under shade of shrubs and trees (shade) than in nearby meadows (sun) where herbivory is intense from the specialist fly Scaptomyza nigrita. This system has served as a textbook example of habitat-biased herbivory driving a plant's distribution across an ecotone, but the proximate mechanisms underlying differential herbivory are still unclear. First, we found that higher S. nigrita herbivory in sun habitats contrasts sharply with their preference to attack plants from shade habitats in laboratory choice experiments. Second, S. nigrita strongly preferred leaves in simulated sun over simulated shade habitats, regardless of plant source habitat. Thus, herbivore preference for brighter, warmer habitats overrides their preference for more palatable shade plants. This promotes the sun-biased herbivore pressure that drives the distribution of bittercress into shade habitats.

Keywords: Brassicaceae; Drosophilidae; bittercress; herbivory; leaf miner; zero-inflated counts.

Fig. 1.

Choice experiments reveal that habitat selection, and not host selection, by foraging Scaptomyza nigrita underlies the pattern of sun-skewed herbivory in nature, despite higher palatability of bittercress from the shade. (A–B) Herbivory is higher on bittercress in sun versus shade habitats, but female S. nigrita prefer shade-grown over sun-grown bittercress when given a choice under uniform lighting. (A) Herbivory field surveys show higher stipples and mines on bittercress in sun vs. shade habitats. (B) Adult female S. nigrita stippled and laid more eggs in bittercress derived from shade versus sun habitats in laboratory choice trials. Statistical results are presented in Table 1. (C–D) Female S. nigrita stippled more (C) and laid more eggs (D) in bittercress leaves in simulated sun compared to shade habitats in field and laboratory choice trials. Choice trials between light and dark sides of assay cages were conducted at two temperatures (see Appendix S4: Fig. S1 for full temperature profiles), indicated below sub-plots. Eggs were counted only for trials in 2015 (see Materials and Methods). Statistical results are presented in Table 1.