Abstract

Interactions among the foraging behaviours of co-occurring animal species can impact population and community dynamics; the consequences of interactions between plant and animal foraging behaviours have received less attention. In North American forests, invasions by European earthworms have led to substantial changes in plant community composition. Changes in leaf litter have been identified as a critical indirect mechanism driving earthworm impacts on plants. However, there has been limited examination of the direct effects of earthworm burrowing on plant growth. Here we show a novel second pathway exists, whereby earthworms (Lumbricus terrestris L.) impact plant root foraging. In a mini-rhizotron experiment, roots occurred more frequently in burrows and soil cracks than in the soil matrix. The roots of Achillea millefolium L. preferentially occupied earthworm burrows, where nutrient availability was presumably higher than in cracks due to earthworm excreta. In contrast, the roots of Campanula rotundifolia L. were less likely to occur in burrows. This shift in root behaviour was associated with a 30% decline in the overall biomass of C. rotundifolia when earthworms were present. Our results indicate earthworm impacts on plant foraging can occur indirectly via physical and chemical changes to the soil and directly via root consumption or abrasion and thus may be one factor influencing plant growth and community change following earthworm invasion. More generally, this work demonstrates the potential for interactions to occur between the foraging behaviours of plants and soil animals and emphasizes the importance of integrating behavioural understanding in foraging studies involving plants.

Highlights

  • Foraging decisions involve integration of multiple environmental cues and are influenced by the presence of other organisms

  • The physical changes in soil structure caused by earthworm burrowing affected both plant species (Figure 2)

  • Roots of A. millefolium (x22 = 85.84, P,0.0001) and C. rotundifolia (x22 = 10.37, P = 0.0056) more frequently occurred in voids than the soil matrix according to mixed effects logistic regression

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Summary

Introduction

Foraging decisions involve integration of multiple environmental cues and are influenced by the presence of other organisms. Root growth of plants is dynamic and is influenced by spatial and temporal heterogeneity in resource distributions [5,6,7] Plants often place their roots preferentially in nutrient patches, species vary in their ability to forage precisely (i.e., concentrate roots in nutrient patches) [8,9]. Though it is broadly recognized that belowground interactions can affect aboveground community structure [14], the mechanisms through which detritivores (as opposed to root-feeding herbivores) influence plants are not well understood [15] Both positive and negative effects of earthworms on plants have been reported, with positive impacts generally occurring in agricultural systems [15]. As a result of this behaviour, biomass of A. millefolium was expected to be more positively affected by the presence of earthworms than C. rotundifolia, unless herbivory by L. terrestris was high

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