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Competition and Predation in Soil Fungivorous Microarthropods Using Stable Isotope Ratio Mass Spectrometry

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Competition and Predation in Soil Fungivorous Microarthropods Using Stable Isotope Ratio Mass Spectrometry fmicb-10-01274 June 6, 2019 Time: 20:12 # 1 ORIGINAL RESEARCH published: 07 June 2019 doi: 10.3389/fmicb.2019.01274 Competition and Predation in Soil Fungivorous Microarthropods Using Stable Isotope Ratio Mass Spectrometry Felicity V. Crotty† and Sina M. Adl* Department of Soil Science, University of Saskatchewan, Saskatoon, SK, Canada The soil food web is often described as having three main energy channels: root, bacterial and fungal. Here we provide quantitative data using a sensitive stable Edited by: isotope ratio mass spectrometry procedure with microcosms on species interactions Stefan Geisen, in the fungal pathway. We measured 15N and 13C enrichment in microarthropods Netherlands Institute of Ecology (NIOO-KNAW), Netherlands through grazing rare isotope enriched fungal mycelia. Experimental treatments were Reviewed by: various combinations of 1, 2, 3, 4 microarthropods species. We used three fungivores Mark Maraun, (the collembolan Lepidocyrtus curvicollis, the Astigmata Tyrophagus putrescentiae, University of Göttingen, Germany Kerstin Heidemann, the Oribatida Oribatula tibialis), and the Mesostigmata predator Hypoaspis acquilifer. University of Göttingen, Germany We collected individuals of each species separately, as well as their feces, and *Correspondence: molt where available. All three fungivorous microarthropods consumed significantly Sina M. Adl more than their own body weight per day. The three fungivores differed in their [email protected] consumption of the mycelium as it was not equally palatable to each. The Mesostigmata †Present address: Felicity V. Crotty, predator Hypoaspis also differed in its microarthropod prey preference. In multiple Royal Agricultural University, species combinations microarthropod behavioral interactions modified consumption Cirencester, United Kingdom and predation rates. Our selection of mites of different sizes, with varied preference Specialty section: for the mycelium, combined with differing predation rates on each mite, demonstrate This article was submitted to that even three trophic level interactions with only five interacting species are not Terrestrial Microbiology, a section of the journal predictably simple. The interpretation of the stable isotope results and consumed- Frontiers in Microbiology excreted weights indicate that: (a) behavior and microscopic observations should not Received: 18 March 2019 be ignored in competition-predation interactions, and (b) functional guilds can take Accepted: 22 May 2019 advantage of more diverse food opportunities. The reality of mixed diets complicates Published: 07 June 2019 functional guild assignments that are reflected in 15N and 13C isotope levels at natural Citation: Crotty FV and Adl SM (2019) abundances in the environment. Microcosm experiments with this sensitive technique Competition and Predation in Soil can help decipher the interpretation of rare isotope natural abundance values, as well as Fungivorous Microarthropods Using Stable Isotope Ratio Mass providing measured consumption, growth, and excretion rate values for modeling soil Spectrometry. food web interactions. Front. Microbiol. 10:1274. doi: 10.3389/fmicb.2019.01274 Keywords: fungivory, microarthropods, nutrient cycling, stable isotopes, trophic interactions Frontiers in Microbiology| www.frontiersin.org 1 June 2019| Volume 10| Article 1274 fmicb-10-01274 June 6, 2019 Time: 20:12 # 2 Crotty and Adl Competition and Predation in Soil Fungivores INTRODUCTION signature can be traced into newly synthesized compounds and tissues (Elfstrand et al., 2008). The introduction of Soil food web models typically recognize three main routes a food source which is enriched above natural abundance energy can flow through the soil – roots, the fungal or bacterial levels with stable isotopes into the soil food web can pathway (Moore et al., 2005). An early study of soil food web elucidate feeding interactions as they are happening. In ecology, structure found that both top-down control and bottom-up shifts in 13C indicate change in diet, and the 13C natural control existed simultaneously and were necessary for ecosystem abundance value indicates an equilibrium average of the stability (de Ruiter et al., 1995). Increased predation rate on various food sources. In contrast 15N values have been used prey, or of grazing consumption (e.g., on bacteria lawn, a to indicate position in trophic level in a food web – the mycelium, or pasture) decreases the biomass and abundance of higher the d 15N value, the higher the trophic level. It also the species consumed, while increasing the abundance of the shows categorically that the food source has been consumed consumers over time. In food webs, the increased abundance and assimilated. or biomass of the consumer trophic level, relative to the However, Maraun et al.(2011) advised there was a need consumed trophic level is called a trophic cascade. It makes to investigate the individual feeding channels, but there is a allusion to the appearance in graphs of successive reduced and difficulty differentiating basal resources using stable isotopes increased biomass in the trophic levels in the system. These at natural abundance. The problem with the interpretation of increasing and decreasing consumption rates oscillate through natural abundance studies with the rare stable isotopes 13C time and ripple through generations and are one cause of and 15N is that it provides an equilibrium and average value population dynamics. An interesting and useful parameter for of all the sources of food consumed (Moore et al., 2004; ecologists is to find out at what relative consumption rates Schneider et al., 2004; Pollierer et al., 2009; Schneider and trophic cascades occur, for they cannot occur under elevated Maraun, 2009). These studies indicated there was sometimes food resources (Polis et al., 2000). It has been postulated that poor resolution between some trophic compartments without the microarthropods, particularly the Collembola and Oribatida, more detailed studies. To address these concerns with natural have a more significant role in the fungal pathway (Faber, abundance field data, it is necessary to turn toward microcosms 1991; Schneider and Maraun, 2005; Jonas et al., 2007). Several to make specific measurements. In these microcosm studies, additional papers discussed fungivory by soil microarthropods it is important to consider both competition and predation (e.g., Maraun et al., 2003; Schneider et al., 2004; Pollierer et al., and not just single species consumption rates, as single species 2009; Thiele-Bruhn et al., 2012), but few tried to quantify results might not be representative of field data (Wardle and rates of hyphae consumption except for individual species, Yeates, 1993). A number of studies employing stable isotopes such as Collembola (Jonas et al., 2007), while others focused focused on quantifying the bacterial energy pathway (e.g., Murray on feeding preferences (e.g., Ruess et al., 2005; Koukol et al., et al., 2009; Crotty et al., 2011b, 2012a), and here this study 2009; Semenina and Tiunov, 2011). However, little is known focuses on the fungal pathway. Tracking the energy flux through regarding the quantities of fungal mycelium consumed and the fungal-feeding channel within soil food webs is more assimilated by microarthropods species when in monoculture, complicated than the bacterial channel (Crotty et al., 2012b). in competition, or with predation pressure. Likewise there Fungi are easily shredded during sampling, and are not easily is little insight into the microarthropods foraging behavior re-introduced in situ, highlighting a need to validate the use of within the soil itself, or their response to the distribution and enriched isotope tracers in microcosm settings to study fungal quality of food resources (Adl, 2003; Hassall et al., 2006). energy pathways. Considering there are 101–102 m of hyphae in one gram Energy flux dynamics in multitrophic interactions food of fertile soil (Leake et al., 2003), this is a large biomass webs provide the data to understand biodiversity-ecosystem contribution to soil nutrient turnover that ought to be studied functioning. Yet, there are few studies portraying this, despite more. The difficulty has been in designing microcosms with the crucial link these studies would provide in linking trophic compatible species, and to develop a technique with sufficient interactions with ecosystem function (Barnes et al., 2018). sensitivity to work with the small number of individuals in a The overall aim of the experiments presented here, were microcosm experiment. to study the effects of species interactions (competition and One of the main methods of differentiating between predation) on the rate of consumption and assimilation as feeding preferences and measuring consumption rates is the determined by isotope ratio mass spectrometry (IRMS). To do use of stable isotopes (Tiunov, 2007; Semenina and Tiunov, this the rate of consumption of saprotrophic fungal biomass 2011), as this can provide a time-integrated measure of by soil microarthropods needed to be determined. We tested the trophic position of soil animals (Pollierer et al., 2009). the hypothesis that mycelium assimilation by the fungivores, An organisms’ tissues exhibit a fixed isotopic enrichment measured as body mass enrichment, will be the same for in relation to their diet; therefore stable isotopes can be each of the species used. We tested the hypothesis that in measured to assess the assimilation rates over the long- the presence of a predator,
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