Root foraging influences plant growth responses to earthworm foraging

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.

Figure 1. Schematic of experimental treatments.

Achillea millefolium and Campanula rotundifolia were grown individually with and without earthworms in 15 replicate pots (27 cm × 11 cm × 26 cm). Three Lumbricus terrestris earthworms were added to each of the earthworm treatment pots. A transparent mini-rhizotron tube (5.7 cm in diameter) ran lengthwise approximately 5 cm below the soil surface of each pot to allow mini-rhizotron images to be obtained. Each mini-rhizotron tube ran through five adjacent pots.

Figure 2. Occurrence of roots (±1 SE) in 6 mm × 6 mm grid cells containing burrows (filled circle), cracks (open circle), and soil (filled inverted triangle) for (A) Achillea millefolium and (B) Campanula rotundifolia over time.

Figure 3. Proportion of 6 mm ×6 mm grid cells with roots dying (± SE), out of all cells occupied by roots during the experiment, in soil, cracks, and burrows for Achillea millefolium and Campanula rotundifolia.

Figure 4. Shoot and root biomass in grams (± SE) for Achillea millefolium and Campanula rotundifolia with and without earthworms.