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

Nicolas M Alexandre,Andrew D Gloss,Henry A Affeldt,Jimmy Lee,Noah K Whiteman,Parris T Humphrey,Joseph Frazier

doi:10.1002/ecs2.2372

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.

Highlights

Abiotic gradients shape fine-scale patterns of plant distributions across the landscape (Whittaker 1967), but consumers, such as insect herbivores, can play a major role as well (Harley 2003, Fine et al 2004, Maron and Crone 2006)
Sun plants had a > 40-fold higher overall leaf mine abundance (3.7 [2.0–6.7] vs. 0.09 [0.03–0.21] mean mines per leaf; P < 0.001; Table 1), and 93% (88–98%) of leaves in shade habitats had no leaf mines at all, compared to only 29% (19–40%) in the sun
We report evidence of a proximate explanation for a textbook case of an herbivore-driven habitat distribution: Insect behavioral taxis strongly biased herbivore foraging toward sun habitats, causing the increased herbivore pressure on sun plants that drives bittercress into the shade

Summary

Introduction

Abiotic gradients shape fine-scale patterns of plant distributions across the landscape (Whittaker 1967), but consumers, such as insect herbivores, can play a major role as well (Harley 2003, Fine et al 2004, Maron and Crone 2006). What distinguishes plant- from herbivorecentric mechanisms is whether the plant or the herbivore response to abiotic gradients takes precedence in shaping realized patterns of herbivore pressure across habitats. Herbivore-centric hypotheses posit that herbivores are more abundant in, or seek out, favorable abiotic habitat conditions (Huffaker and Kennett 1959), independent of how plant traits vary across habitats. In this case, herbivore habitat tolerance and/or preference is directly shaped by abiotic conditions, which creates enemy-free space exploitable by plants. We addressed how plant- vs herbivore-centric factors impact the habitat-specific herbivory pressure that is responsible for shaping the habitat distribution of a native subalpine plant

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