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Nematode Functional Guilds, Not Trophic Groups, Reflect Shifts in Soil

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Nematode Functional Guilds, Not Trophic Groups, Reflect Shifts in Soil Pedobiologia 58 (2015) 23–32 Contents lists available at ScienceDirect Pedobiologia - Journal of Soil Ecology j ournal homepage: www.elsevier.de/pedobi Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors a,b,c,∗ d,e a f Simone Cesarz , Peter B. Reich , Stefan Scheu , Liliane Ruess , a b,c Matthias Schaefer , Nico Eisenhauer a J.F. Blumenbach Institute of Zoology and Anthropology, Georg August University Göttingen, Berliner Straße 28, 37073 Göttingen, Germany b German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany c Institute of Biology, University of Leipzig, Johannisallee 21, 04103 Leipzig, Germany d Department of Forest Resources, University of Minnesota, 1530 Cleveland Avenue North, St. Paul, MN 55108, USA e Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, NSW 2751, Australia f Institute of Biology, Humboldt University Berlin, Philippstr. 13, 10115 Berlin, Germany a r t i c l e i n f o a b s t r a c t Article history: Soils store ∼80% of global terrestrial organic carbon and alterations in fluxes into and out of this pool Received 29 September 2014 may interact with ongoing climate change. Belowground food webs drive soil C dynamics, but little is Received in revised form 7 January 2015 known about their responses to co-occurring global change agents. We investigated open-air experi- Accepted 7 January 2015 mental grassland communities at ambient and elevated atmospheric CO2 concentration, ambient and enriched nitrogen input, and ambient and reduced summer precipitation to evaluate how these agents Keywords: interactively affect soil nematodes, which are often used as an indicator group for soil food web structure Nematodes and soil health. The aim of the study was to elucidate the response of the functional diversity of soil Food web complexity nematodes to changing environmental conditions by using nematode functional guilds and indices as Global change Grassland indicators. Soil processes The results suggest that nematode functional guilds surpass nematode trophic groups as soil indicators, Taxonomical resolution suggesting that more detailed data on nematode community structure is essential to capture functional changes in response to environmental change. For instance, the density of opportunistic fungal feeders increased due to N addition with the response being more pronounced at elevated CO2, whereas densities of sensitive fungal-feeders were increased at ambient N and elevated CO2, illustrating opposing responses within one trophic group. Opportunistic bacterial feeders increased at elevated N, but did not respond to other environmental factors studied. Root-feeding Longidoridae were significantly reduced at elevated CO2 and elevated N compared to ambient conditions, whereas other plant feeders were little affected by the manipulations. Predacious nematodes were less abundant at elevated N, and the Structure Index (which indicates food web structure) suggested reduced top-down forces and simplified soil food webs, although omnivores did not vary significantly. Elevated CO2 buffered the effect of reduced precipitation on the Enrichment Index (which indicates increased resource availability) and the Channel Index (which indicates changes in decomposition channel) probably due to reduced stomatal conductance at elevated CO2. Further, the results suggest that the decomposer community switched from a bacterial-dominated to a fungal-dominated system at elevated N, indicating shifts in the microbial community as well as in the functioning of belowground food webs. Overall, the studied global change agents interactively and differentially affected functional guilds of soil nematodes, suggesting complex changes in soil processes. We highlight that detailed information on the functional guilds of nematodes is likely necessary to fully understand alterations in soil food webs and related processes due to global environmental change. © 2015 Elsevier GmbH. All rights reserved. ∗ Corresponding author at: German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany. Tel.: +49 341 9733174. E-mail address: [email protected] (S. Cesarz). http://dx.doi.org/10.1016/j.pedobi.2015.01.001 0031-4056/© 2015 Elsevier GmbH. All rights reserved. 24 S. Cesarz et al. / Pedobiologia 58 (2015) 23–32 Introduction In addition to altered CO2 and N levels, climate is projected to change with altered precipitation regimes (IPCC 2007; Kerr 2007). Human activities lead to changes in atmospheric CO2 concen- Soil moisture and related biotic and abiotic parameters are impor- trations, nitrogen (N) deposition, and precipitation regimes with tant driving forces for soil processes (Kardol et al. 2010). Drought considerable impacts on ecosystem functioning (IPCC 2007). These has mostly negative effects on soil fauna by decreasing directly global change agents are acting in concert, and understanding their reproduction and development (Lindberg et al. 2002) or indi- their interactive effects is crucial to predict the consequences rectly by changing the composition and biomass of microorganisms for ecosystem functions and services (Reich et al. 2006a). Typi- (Hawkes et al. 2011) and plants (Kardol et al. 2010). In addition, cally, in terrestrial ecosystems >90% of the biomass produced by responses to changes in soil moisture regimes depend on the plant plants enters the dead organic matter pool forming the basis of the community (Gross et al. 2008). Soil moisture may interact with decomposer system (Schlesinger and Andrews 2000). Thus, under- CO2 and N availability because elevated CO2 levels often increase standing interactions between plants and decomposers is of high soil water content and N content increases with higher soil mois- importance, especially as the balance between carbon sequestra- ture (Körner 2000; Zhang and Wienhold 2002); therefore, complex tion and carbon loss depends on those interrelationships (Gessner interactions in soil processes and involved soil biota are likely. et al. 2010) as well as on interactions between global change agents Recently, Reich et al. (2014) showed highest biomass production (Zaehle 2013). at elevated CO2, elevated N and ambient rain (not removed) and Since the industrial revolution, CO2 concentrations in the atmo- revealed complex relationships that, e.g., a lacking CO2 effect may sphere have increased from approximately 270 ppm to 380 ppm be due to other limiting nutrients and moisture conditions. Most in 2005 and presumably will reach 550 ppm by the year 2050 previous studies were based only on short-term experiments and (IPCC 2007; Rogelj et al. 2012). Higher atmospheric CO2 concen- separately investigated global change agents (Blankinship et al. trations significantly impact plant physiological processes. At least 2011). Although these studies provided important insights into three responses are relevant to the decomposer system. Most the mechanisms underlying main effects, interactions between co- prominent is the increase in plant carbon (C) acquisition, which occurring global change agents have to be considered to get more leads to both greater biomass production (Ainsworth and Long realistic predictions of future changes. 2005) and greater inputs of labile C forms to the soil (Adair et al. One promising approach to detect changes in soil processes is 2011). Also, increasing C acquisition is usually associated with a the investigation of soil food web structure, exemplified by the larger C-to-N ratio of live plant tissue, and, therefore, reduced tis- composition of functional guilds of nematodes (Bongers 1990; sue quality for consumers (Körner 2000). These plant responses Yeates et al. 1993; Ferris et al. 2001). As nematodes have diverse have cascading effects on both aboveground (Lau and Tiffin 2009) feeding behaviors and life strategies and play a key role in soil and belowground consumers (Blankinship et al. 2011), the latter food webs, they function as important indicators for ecosystem representing important drivers of soil processes, such as organic processes (Ferris 2010; Yeates 2010). Functional grouping of nema- matter decomposition and nutrient mineralization. Belowground todes provides important information to detect changes in soil responses to higher plant biomass production and rhizodeposi- processes by considering distinct feeding strategies, e.g., bacterial tion under elevated atmospheric CO2 can either increase C loss or fungal-feeding in combination with their responses (tolerance by increasing bottom-up forces leading to increased decomposi- vs. sensitivity) to environmental changes. In addition, nematode- tion or enhance C sequestration when top-down forces counter based indices allow the evaluation of ecosystem nutrient status bottom-up forces (Wardle et al. 1998; Schulze and Freibauer 2005). (enriched vs. depleted), structure of the soil food web (complex- This balance has major implications for ecosystem feedback effects ity vs. simplicity), and the relevance of decomposition channels on atmospheric CO2 concentrations and therefore on the global (bacterial vs. fungal) (Ferris et al. 2001). C cycle, and may depend on other co-occurring global change We used a well-established global change experiment in grass- agents, such as N inputs (Hoeksema et al. 2000; Chung et al. land (BioCON; Reich et al. 2001a,b,c) to explore interactive effects
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