Scavenging beetles control the temporal response of soil communities to carrion decomposition

Marco O Ilardi,Tancredi Caruso,Sheena C Cotter,Edith C Hammer,Gillian Riddell

doi:10.1111/1365-2435.13849

Abstract

Abstract Carrion is a frequent but overlooked source of nutrients to the soil. The decomposition of carrion is accelerated by invertebrate scavengers, but the impact of the scavengers on below‐ground biota and its functions is scarcely known. We conducted a laboratory experiment to investigate the effects of the burying beetle Nicrophorus vespilloides on the soil community of a temperate broadleaved forest. We assembled microcosms from soil collected from an oak woodland and treated them with mouse Mus musculus carcasses and mating pairs of burying beetles (♀+♂) in a factorial design with control soils. We sampled independent replicates over time to investigate how the beetles affect soil microarthropods and microbial biomass (bacteria and fungi) in relation to soil pH and organic matter content. The beetle treatment initially reduced the total microbial biomass and abundance of major groups of microarthropods relative to the control soil. At the same time, organic matter increased in the beetle treatment and then dropped to the pre‐beetle level (i.e. soil baseline) at the end of the beetle breeding cycle (2 weeks). The rapid temporal changes in organic matter were mimicked by the relative abundances of the dominant microarthropod groups, with Oribatida relatively more abundant than Collembola and predaceous mites in the beetle treatment. The overall final effect of the beetle (relative to the laboratory control) on microarthropods was negative but the beetle kept these variables within the levels observed for freshly collected soil (baseline), while the final effect on pH was positive, and most likely driven by the surplus of nutrients from the carcass and biochemical changes triggered by the decomposition process. In nature, scavenging invertebrates are widespread. Our study demonstrates that beetles breeding in carcasses regulate the dynamics of key components of the soil food web, including microbial biomass, changes in the relative abundances of dominant microarthropods and soil organic matter and pH. Given the abundance of these beetles in nature, the study implies that the distribution of these beetles is a key driver of variation in soil nutrient cycling in woodlands. A free Plain Language Summary can be found within the Supporting Information of this article.

Highlights

Terrestrial ecosystems consist of functionally coupled above-ground and below-ground ecological communities (Bardgett et al, 2005; Bardgett & Wardle, 2010; Van der Putten et al, 2001)
Our study demonstrates that beetles breeding in carcasses regulate the dynamics of key components of the soil food web, including microbial biomass, changes in the relative abundances of dominant microarthropods and soil organic matter and pH
Most of the research investigating above-ground–below-ground linkages has focused on plant–soil interactions because the bulk of soil organic matter consists of dead plant material and rhizodeposits (Coleman et al, 2004; Lehmann & Kleber, 2015) but in some terrestrial ecosystems, such as broadleaved forests, the carcasses of above-ground fauna, like micromammals and small passerines, arguably represent a constant input of organic matter (Barton et al, 2013, 2016; Carter et al, 2007)

Summary

| INTRODUCTION

Terrestrial ecosystems consist of functionally coupled above-ground and below-ground ecological communities (Bardgett et al, 2005; Bardgett & Wardle, 2010; Van der Putten et al, 2001). When carrion is not directly consumed and removed by opportunistic saprophagous or necrophagous vertebrates (DeVault et al, 2011; Henrich et al, 2017; Young et al, 2014), they create islands of surplus nutrients, which are nearly always colonized by various invertebrate taxa These invertebrates use carcasses as a food source and/or breeding substrate, accelerating the decomposition process (Barton & Evans, 2017; Blackith & Blackith, 1990; Trumbo et al, 2016; Yang, 2006). In either slow or accelerated decomposition, there is a considerable amount of organic matter being released into the soil, which represents a substantial increase in nitrogen, phosphorous and other nutrients for the soil ecosystem and the associated plant community (Barton et al, 2016; Parmenter & MacMahon, 2009) Such significant input of nutrients, exudates and antimicrobial chemicals is bound to affect the surrounding soil and its biota, but studies are lacking. We hypothesized that changes in the soil (biotic and abiotic) will vary over time as a function of the key steps in the breeding cycle of beetle (see Figure 1 for a graphical summary of key hypotheses and findings)

| MATERIALS AND METHODS

Baseline

Findings

| DISCUSSION

| CONCLUSIONS