Aphid honeydew-induced changes in soil biota can cascade up to tree crown architecture

• The effect of aphid honeydew on soil biota and tree performance was investigated.
• Aphid honeydew altered tree resource allocation and crown architecture.
• Aphid honeydew also induced changes in soil fauna.
• Path analyses suggest changes in tree resource allocation mediated by soil fauna.

It has been hypothesised that aphid honeydew could alleviate the feeding damage by aphids via changes in soil biota leading to increased nutrient cycling and plant nutrient availability. However, to date, the evidence is equivocal. We used a field experiment with willow saplings to investigate the effect of aphid honeydew on trees with and without simulated honeydew deposition. Specifically, here we tested whether: (1) honeydew deposition can trigger changes in soil biota community composition, and (2) honeydew-induced changes in soil biota cascade up to affect plant performance and resource allocation. Honeydew deposition significantly increased microbial biomass and respiration, microfauna densities, earthworm biomass and litter mineralisation kinetics, while having detrimental effects on Collembola and mites. Honeydew deposition also increased the tree shoot to root biomass ratio and altered the crown canopy architecture and flowering phenology. However, no effects on leaf nitrogen content and tree shoot or root biomass were found. This was likely due to increased microbial nutrient immobilisation under the honeydew treatment. Path analyses present supporting evidence that the honeydew-induced changes in soil biota (notably via a pathway from microbial biomass to endogenic earthworms), can cascade up to affect tree resource allocation and crown architecture.