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Field Exclusion of Large Soil Predators Impacts Lower Trophic Levels, And

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DR NEREIDA MELGUIZO-RUIZ (Orcid ID : 0000-0001-5153-5281) DR AMY T AUSTIN (Orcid ID : 0000-0002-7468-5861) Article type : Research Article Handling Editor: Dr Natalie Clay Field exclusion of large soil predators impacts lower trophic levels, and decreases leaf-litter decomposition in dry forests Nereida Melguizo-Ruiz 1,2,3, Gerardo Jiménez-Navarro 1,3, Eva De Mas 1, Joaquina Pato2, Stefan Scheu 4,5, Amy T. Austin 6, David H. Wise 7 and Jordi Moya-Laraño 1 1 Estación Experimental de Zonas Áridas, Functional and Evolutionary Ecology, Consejo Superior de Investigaciones Científicas (CSIC), La Cañada de San Urbano, Almería, Spain. 2 Research Unit of Biodiversity (UO/CSIC/PA), Oviedo University, Mieres, Spain. 3 CIBIO/InBio Research Center in Biodiversity and Genetic Resources, 7000-651, Évora, Portugal. 4 J.F. Blumenbach Institute of Zoology and Anthropology, Animal Ecology, University of Göttingen, Göttingen, Germany. 5 Centre of Biodiversity and Sustainable Land Use, University of Göttingen, Göttingen, Germany. 6 Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Agronomía, Universidad de Buenos Aires, Buenos Aires, Argentina. This article has been accepted for publication and undergone full peer review but has not been through the copyediting,Accepted Article typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/1365-2656.13101 This article is protected by copyright. All rights reserved 7 Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois, United States. Corresponding author: Nereida Melguizo-Ruiz, CIBIO-InBIO, Research Center in Biodiversity and Genetic Resources, Casa Cordovil, Rua Dom Augusto Eduardo Nunes 7000-651, Evora, Portugal. E- mail: [email protected]. Accepted Article This article is protected by copyright. All rights reserved Abstract 1. Shifts in densities of apex predators may indirectly affect fundamental ecosystem processes, such as decomposition, by altering patterns of cascading effects propagating through lower trophic levels. These top-down effects may interact with anthropogenic impacts, such as climate change, in largely unknown ways. 2. We investigated how changes in densities of large predatory arthropods in forest leaf-litter communities altered lower trophic levels and litter decomposition. We conducted our experiment in soil communities that had experienced different levels of long-term average precipitation. We hypothesized that altering abundances of apex predators would have stronger effects on soil communities inhabiting dry forests, due to lower secondary productivity and greater resource overexploitation by lower trophic levels compared to wet forests. 3. We experimentally manipulated abundances of the largest arthropod predators (apex predators) in field mesocosms replicated in the leaf-litter community of Iberian beech forests that differed in long-term mean annual precipitation by 25% (three dry forests with MAP < 1250 mm and four wet forests with MAP > 1400 mm). After one year, we assessed abundances of soil fauna in lower trophic levels and indirect impacts on leaf-litter decomposition using litter of understory hazel, Corylus avellana. 4. Reducing densities of large predators had a consistently negative effect on final abundances of the different trophic groups and several taxa within each group. Moreover, large predatory arthropods strongly impacted litter decomposition, and their effect interacted with the long-term annual rainfall experienced by the soil community. In the dry forests, a 50% reduction in the densities of apex predators was associated with a 50% reduction in decomposition. In wet forests, the same reduction in densities of apex soil predators did not alter the rate of litter decomposition. 5. Our results suggest that predators may facilitate lower trophic levels by indirectly reducing competition and resource overexploitation, cascading effects that may be more pronounced in drier forests where conditions have selected for greater competitive ability and more rapid resource utilization. These findings thus provide insights into the functioning of soil invertebrate communities and their role in decomposition, as well as potential consequences of soil community responses to climate change. Accepted Article This article is protected by copyright. All rights reserved KEYWORDS Apex predators; body size; climate change; field mesocosms; leaf-litter decomposition; precipitation; soil food webs; top-down control Accepted Article This article is protected by copyright. All rights reserved Changes in the densities of large apex consumers (top predators) may strongly affect ecosystem structure and dynamics (Duffy, 2003; Schmitz, Hawlena, & Trussell, 2010). These effects may interact with other anthropogenic impacts such as climate change, alterations in land use, and habitat loss; therefore, understanding the role of top predators in food webs and their interactions with environmental drivers may be central to predicting the consequences of biodiversity loss in ecosystem functioning. Trophic cascades, which occur when consumer impacts propagate through lower trophic levels, may lead to strong ecosystem-level effects (see Pace et al., 1999 for a review). Predators can indirectly affect ecosystem processes such as primary productivity (Schmitz, Hambäck, & Beckerman, 2000; Halaj & Wise, 2001) and litter decomposition (Kajak, 1995; Lawrence & Wise, 2004; Koltz, Classen, & Wright, 2018). These indirect effects of predators can be mediated by changes in population densities of lower trophic levels, i.e. density-mediated indirect interactions (DMII); or by changes in specific behaviours of lower levels, i.e. behavioural or trait-mediated indirect interactions (TMII) (see Werner & Peacor 2003 for a review). The pattern of results to date is complex, as the sign of the predator-induced cascades can vary from negative to neutral to positive, suggesting that factors such as abiotic conditions may strongly influence the nature of the trophic cascade (Chase, 1996; Lawrence & Wise, 2004; Lensing & Wise, 2006; Wu et al., 2011; Kardol et al., 2016; McCluney & Sabo, 2016). Furthermore, not all effects may propagate to lower trophic levels or affect ecosystem processes in all systems. There are compensatory mechanisms that can dampen, minimize and even suppress cascades, such as trophic-level omnivory or the regulation of other trophic levels not predicted by cascading trophic interactions (Pace et al., 1999). In particular, intraguild predation (Polis et al., 1989) can complicate the influence of top-down patterns on lower trophic levels (Finke & Denno, 2005), since generalist predators have the capacity not only to directly reduce prey densities, but also to indirectly increase the abundance of lower trophic levels by preying on other natural enemies (e.g. Snyder & Wise 2001). Accepted Article This article is protected by copyright. All rights reserved Manipulative field experiments to uncover the nature of trophic cascades have removed or added one or more taxa (e.g. Lawrence & Wise, 2004), or have manipulated abundances of predators with different functional attributes or foraging strategies (such as web-building and hunting spiders and ants, Sanders et al., 2011). To our knowledge no study has altered the density of an entire size- defined trophic functional group. Because predators are usually larger than their prey (Schneider & Brose, 2013), the top (apex) predators are often the largest in the system (Woodward et al., 2005). Thus, manipulating abundances of the largest predators from a natural food web could reveal the cascading indirect effects of such apex predators on decomposition rates, through changes in abundances of lower trophic levels. As apex predators are more sensitive to climate change, they tend to be the first organisms lost in food webs. This is probably due to their relatively higher metabolic requirements and smaller population sizes; or owing to bottom–up effects, i.e. top predators may be the most sensitive to the lowered productivity in the basal trophic level (Petchey et al., 1999; Voigt et al., 2003; Gilman et al., 2010). Therefore, it becomes urgent to understand how changes in densities of apex predators could interact with climate to impact other trophic levels and associated ecosystem processes. This is particularly important in soil ecosystems and their upper layer, the leaf-litter food web, because we know little about how biotic interactions from top predators to basal resources (Fig. 1) interact with abiotic factors to determine the rate of leaf-litter decomposition (but see Lensing & Wise, 2006). Climate-change predictions focus on both increases in global temperature and changes in rainfall patterns (Stocker et al., 2013), with an expected decrease in precipitation in several parts of the earth. In soil ecosystems, water availability resulting from short-term precipitation patterns can indirectly impact how trophic cascades affect decomposition. Drier soil conditions during droughts appear to strongly affect fungal growth (A'Bear, Jones, & Boddy, 2014), which in turn may alter how trophic cascades affect rates of litter decomposition through the activity of fungivores (Lensing & Wise, 2006). For instance, intermediate levels of fungal grazing by springtails can stimulate
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