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Greenop Ecology Manuscript R2.Pdf Patron: Her Majesty The Queen Rothamsted Research Harpenden, Herts, AL5 2JQ Telephone: +44 (0)1582 763133 WeB: http://www.rothamsted.ac.uk/ Rothamsted Repository Download A - Papers appearing in refereed journals Greenop, A., Woodcock, B. A., Wilby, A., Cook, S. M. and Pywell, R. F. 2018. Functional diversity positively affects prey suppression by invertebrate predators: a meta-analysis. Ecology. 99 (8), pp. 1771-1782. The publisher's version can be accessed at: • https://dx.doi.org/10.1002/ecy.2378 The output can be accessed at: https://repository.rothamsted.ac.uk/item/8471z. © 4 May 2018, Rothamsted Research. Licensed under the Creative Commons CC BY. 11/03/2019 13:57 repository.rothamsted.ac.uk [email protected] Rothamsted Research is a Company Limited by Guarantee Registered Office: as above. Registered in England No. 2393175. Registered Charity No. 802038. VAT No. 197 4201 51. Founded in 1843 by John Bennet Lawes. Ecology Functional diversity positively affects prey suppression by invertebrate predators: a meta-analysis Journal: Ecology ManuscriptFor ID ECY17-0800.R2 Review Only Wiley - Manuscript type: Articles Date Submitted by the Author: 23-Feb-2018 Complete List of Authors: Greenop, Arran; Centre for Ecology and Hydrology, ; Lancaster Environment Centre, Woodcock, Ben; CEH Wilby, Andrew; Lancaster University Cook, Sam; Rothamsted Research Pywell, Richard; Centre for Ecology and Hydrology, UK Predation < Species Interactions < Community Ecology < Substantive Area, Biological Control < Species Interactions < Community Ecology < Substantive Area: Substantive Area, Agroecosystems < Ecosystems < Substantive Area, Phylogenetics < Systematics < Population Ecology < Substantive Area, Species Interactions < Community Ecology < Substantive Area Organism: Habitat: Geographic Area: Functional diversity, Phylogenetic diversity, Predator-prey interactions, Traits, Conservation biological control, Natural enemies, Biodiversity and Additional Keywords: ecosystem functioning, Agricultural ecosystems, Ecosystem services, Species richness The use of pesticides within agricultural ecosystems has led to wide concern regarding negative effects on the environment. One possible alternative is the use of predators of pest species that naturally occur within agricultural ecosystems. However, the mechanistic basis for how species can be manipulated in order to maximise pest control remains unclear. We carried out a meta-analysis of 51 studies that manipulated predator species richness in reference to suppression of herbivore prey to Abstract: determine which components of predator diversity affect pest control. Overall, functional diversity (FD) based on predator’s habitat domain, diet breadth and hunting strategy was ranked as the most important variable. Our analysis showed that increases in FD in polycultures led to greater prey suppression compared to both the mean of the component predator species, and the most effective predator species, in monocultures. Further analysis of individual traits indicated these effects are likely to be driven by Page 1 of 94 Ecology broad niche differentiation and greater resource exploitation in functionally diverse predator communities. A decoupled measure of phylogenetic diversity, whereby the overlap in variation with FD was removed, was not found to be an important driver of prey suppression. Our results suggest that increasing FD in predatory invertebrates will help maximise pest control ecosystem services in agricultural ecosystems, with the potential to increase suppression above that of the most effective predator species. For Review Only Ecology Page 2 of 94 1 Running head: Functional diversity drives prey suppression 2 Functional diversity positively affects prey suppression by invertebrate predators: a 3 meta-analysis 4 Arran Greenop. 1,2, Ben A Woodcock1, Andy Wilby 2, Samantha M Cook 3 & Richard F 5 Pywell 1. 6 1 NERC Centre for Ecology & Hydrology, Maclean Building, Crowmarsh Gifford, 7 Wallingford, Oxfordshire OX10 8BB, UK. Tel. +44(0)1491692415 8 2 Lancaster EnvironmentFor Centre, LibraryReview Avenue, Lancaster Only University, Lancaster LA1 4YQ 9 3 Biointeractions and Crop Protection Department, Rothamsted Research, Harpenden, Herts, 10 AL5 2JQ, UK. 11 12 Contact Author: Arran Greenop, e-mail:[email protected], 07538808379 13 14 15 16 17 18 19 20 21 22 23 24 25 1 Page 3 of 94 Ecology 26 Abstract 27 The use of pesticides within agricultural ecosystems has led to wide concern regarding 28 negative effects on the environment. One possible alternative is the use of predators of pest 29 species that naturally occur within agricultural ecosystems. However, the mechanistic basis 30 for how species can be manipulated in order to maximise pest control remains unclear. We 31 carried out a meta-analysis of 51 studies that manipulated predator species richness in 32 reference to suppression of herbivore prey to determine which components of predator 33 diversity affect pest control.For Overall, Review functional diversity Only (FD) based on predator’s habitat 34 domain, diet breadth and hunting strategy was ranked as the most important variable. Our 35 analysis showed that increases in FD in polycultures led to greater prey suppression 36 compared to both the mean of the component predator species, and the most effective 37 predator species, in monocultures. Further analysis of individual traits indicated these effects 38 are likely to be driven by broad niche differentiation and greater resource exploitation in 39 functionally diverse predator communities. A decoupled measure of phylogenetic diversity, 40 whereby the overlap in variation with FD was removed, was not found to be an important 41 driver of prey suppression. Our results suggest that increasing FD in predatory invertebrates 42 will help maximise pest control ecosystem services in agricultural ecosystems, with the 43 potential to increase suppression above that of the most effective predator species. 44 45 46 Key words: Functional diversity, Phylogenetic diversity, Predator-prey interactions, Traits, 47 Conservation biological control, Natural enemies, Biodiversity and ecosystem functioning, 48 Agricultural ecosystems, Ecosystem services, Species richness 49 50 2 Ecology Page 4 of 94 51 Introduction 52 The predicted growth of global populations will lead to an ever-increasing demand for 53 agricultural systems to deliver greater food production (25% - 75% increase in food by 2050; 54 Hunter et al, 2017). Whilst this goal may be achieved through conventional forms of 55 agricultural intensification, there are likely limitations to the extent to which chemical 56 insecticides can be relied upon without facing a myriad of risks. These range from the 57 likelihood of pesticide resistance in pest species (Nauen & Denholm 2005; Bass et al. 2014), 58 the revocation of active Foringredients Review (NFU, 2014), damaging Only effects on non-target organisms 59 (Easton & Goulson 2013; Hallmann et al. 2014; Woodcock et al. 2016, 2017), as well as diffuse 60 pollution impacting on human and environmental health in general (Wilson & Tisdell 2001; 61 Horrigan et al. 2002). An increased reliance on conservation biological control, where 62 predators or parasitoids (here, referred to collectively as predators) of pest species are 63 encouraged within agricultural ecosystems has the potential to address some of these issues 64 (Begg et al. 2017). Fundamental to integrating conservation biological control into agricultural 65 practices is understanding which components of invertebrate biodiversity need to be managed 66 to maximise pest suppression. 67 68 A number of meta-analyses (Bianchi et al. 2006; Letourneau et al. 2009; Griffin et al. 2013) 69 have demonstrated that higher predator richness can increase prey suppression (reduction in 70 herbivores by predators), however, species richness provides little elucidation as to the 71 underlying mechanisms driving this trend. An important characteristic of multi-predator 72 systems is the presence of significant variation in the response of prey suppression to increasing 73 predator species richness; a consequence of the range of complex interactions between 74 predators, and predators and prey (Ives et al. 2004; Casula et al. 2006; Schmitz 2007). For 75 example, intraguild interactions can be positive (functional facilitation), whereby predators 3 Page 5 of 94 Ecology 76 facilitate the capture of prey by other predator species (Losey & Denno 1998). Niche 77 complementarity is another interaction that can lead to overyielding of prey suppression by 78 diverse assemblages, where individual predators may feed on different life stages of a prey 79 species (Wilby et al. 2005). However, negative interactions also occur between predators 80 reducing prey suppression in diverse assemblages. One of the most commonly encountered of 81 these is intraguild predation, whereby a top predator consumes not only the prey but also the 82 intermediate predators (Rosenheim et al. 2004a; Finke & Denno 2005). Interference 83 competition can also occurFor whereby Review one predator species Only reduces prey capture by the other due 84 to negative behavioural interactions (Lang 2003). Given the complexity of these interactions, 85 the net effect of predator species diversity is often difficult to predict. 86 87 Defining morphological or behavioral characteristics of individual species that potentially 88 impact on prey suppression, often referred to as functional effect traits, provides an opportunity 89 to elucidate
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