Aphid honeydew-induced changes in soil biota can cascade up to tree crown architecture Alexandru Milcu a,b, *, Michael Bonkowski c , C. Matilda Collins d , Michael J. Crawley e a CEFE-CNRS, UMR 5175, Université de Montpellier – Université Paul Valéry – EPHE, CNRS, 1919 route de Mende, F-34293 Montpellier Cedex 5, France b CNRS Ecotron, UPS 3248, Campus Baillarguet, 34980, Montferrier-sur-Lez, France c Department of Terrestrial Ecology, Institute for Zoology, University of Cologne, Zülpicher Str. 47b, 50674 Köln, Germany d Centre for Environmental Policy, Imperial College London, SW7 2NA, UK e Imperial College London, Silwood Park, Ascot, Berkshire SL5 7PY, UK A R T I C L E I N F O Article history: Received 28 May 2015 Received in revised form 24 July 2015 Accepted 25 July 2015 Keywords: Plant–soil interactions Plant–herbivore interactions Soil fauna Earthworms Tuberolachnus salignus Willow A B S T R A C T 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. ã 2015 Elsevier GmbH. All rights reserved. 1. Introduction Herbivory by aphids is commonly associated with the deposi- tion of a substantial amount of sugary excretes, known as honeydew. It has been hypothesized that honeydew deposition resulting from aphid feeding can mitigate or compensate for the negative direct effects of herbivory (Choudhury, 1984; Owen, 1980). A positive feedback loop involving changes in soil biota leading to increased nutrient cycling and plant nutrient availability was first hypothesized by Owen and Wiegert (1976) as an indirect compensatory mechanism. However, the evidence is far from equivocal. To date, there is evidence that the readily available carbon (C) present in honeydew can increase the total supply of nitrogen via stimulation of free-living nitrogen-fixing soil bacteria (Petelle, 1984, 1980, 1981), reduce the amount of nitrogen in soil leachate (Stadler et al., 2006, 1999), increase microbial biomass and activity (Dighton, 1978; Choudhury, 1985), and may trigger bottom-up cascading effects on soil food webs (Seeger and Filser, 2008; Wardle et al., 2010). Yet, several studies found no support for a soil biota mediated positive feedback loop (Foster, 1984; Grier and Vogt, 1990; Wardhaugh and Didham, 2006), suggesting that the magnitude and direction of these effects may depend on the attributes of the interacting species. Alternatively, it has been hypothesised that the alleviation of C limitation by honeydew deposition could lead to increased belowground inter-kingdom competition for the next limiting macronutrient, which often is nitrogen (Kaye and Hart, 1997). This was proposed to be an important mechanism controlling plant nutrient availability, with some supporting evidence showing a substantial reduction in soil nitrogen availability, leading to lower leaf nitrogen concentrations and biomass production under aphid infested alder trees (Grier and Vogt, 1990). However, it remains unclear what are the honeydew-mediated indirect effects of aphid feeding and whether the hypothesised positive feedback loop involving changes in soil biota and soil nutrient availability contributes to mitigate the negative direct effects of aphid feeding (Grier and Vogt, 1990; * Corresponding author at: CNRS Ecotron, UPS 3248, Campus Baillarguet, 34980, Montferrier-sur-Lez, France. E-mail address: alex.milcu@cnrs.fr (A. Milcu). http://dx.doi.org/10.1016/j.pedobi.2015.07.002 0031-4056/ ã 2015 Elsevier GmbH. All rights reserved. Pedobiologia xxx (2015) xxx–xxx G Model PEDOBI 50439 No. of Pages 9 Please cite this article in press as: Milcu, A., et al., Aphid honeydew-induced changes in soil biota can cascade up to tree crown architecture. PEDOBI (2015), http://dx.doi.org/10.1016/j.pedobi.2015.07.002 Contents lists available at ScienceDirect Pedobiologia - Journal of Soil Ecology journal homepa ge: www.elsev ier.de/pe dobi