Soil engineering by ants facilitates plant compensation for large herbivore removal of aboveground biomass

The interplay between top-down and bottom-up processes determines
ecosystem productivity. Yet, the factors that mediate the balance between
these opposing forces remain poorly understood. Furthering this challenge,
complex and often cryptic factors like ecosystem engineering and
trait-mediated interactions may play major roles in mediating the outcomes
of top-down and bottom-up interactions. In semi-arid grasslands of
northeastern China, we conducted a large-scale, three-year experiment to
evaluate how soil engineering by ants and plasticity in
plants independently and jointly influenced the top-down effects
of grazing by a ubiquitous herbivore (cattle) on aboveground
standing biomass of the dominant perennial grass, Leymus chinensis.
Herbivory had strong top-down effects, reducing L. chinensis AB
by 25% relative to baseline levels without cattle or ants. In contrast,
soil engineering by ants facilitated weak bottom-up effects in the absence
of herbivory. However, in the presence of herbivory, soil engineering
effects were strong enough to fully offset herbivore removal of
aboveground biomass. This outcome was mediated by L. chinensis’s
plasticity in reallocating growth from below- to aboveground biomass, a
result linked to additive effects of engineers and herbivores increasing
soil N availability and engineering effects improving soil structure. Soil
engineering increased soil N by 12%, promoting aboveground biomass.
Herbivores increased soil N by 13% via defecation, but this increase
failed to offset their reductions in aboveground biomass in isolation.
However, when combined, engineers and herbivores increased soil N by 26%
and engineers improved soil bulk density, facilitating L.
chinensis to shift resource allocations from below- to
aboveground biomass sufficiently to fully offset herbivore suppression of
aboveground biomass. Our results demonstrate that soil engineering and
trait-mediated effects of plant plasticity can strongly mediate the
outcome of top-down and bottom-up interactions. These cryptic but perhaps
ubiquitous processes may help to explain the long-debated phenomenon of
plant compensatory responses to large grazers.