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Downtown Diet: a Global Meta-Analysis of Urbanization on Consumption Patterns of Vertebrate

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Downtown Diet: a Global Meta-Analysis of Urbanization on Consumption Patterns of Vertebrate bioRxiv preprint doi: https://doi.org/10.1101/2020.12.19.423628; this version posted December 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. In review at Ecology Letters (December 2020) 1 Downtown Diet: a global meta-analysis of urbanization on consumption patterns of vertebrate 2 predators 3 4 Siria Gámez1*, Abigail Potts2*, Kirby L. Mills1, Aurelia A. Allen2, Allyson Holman3, Peggy 5 Randon2, Olivia Linson4, and Nyeema C. Harris1 6 7 1Applied Wildlife Ecology Lab, Ecology and Evolutionary Biology, University of Michigan 8 1101 N. University Ave, Ann Arbor, Michigan 48106 9 2 Ecology and Evolutionary Biology, University of Michigan 1101 N. University Ave, Ann 10 Arbor, Michigan 48106 11 3 Rackham Graduate School, University of Michigan 915 E Washington St, Ann Arbor, 12 Michigan 48109 13 4 College of Literature, Science and the Arts, University of Michigan 500 S State ST #2005, Ann 14 Arbor, Michigan 48109 15 *these authors contributed equally 16 17 18 Corresponding author: Siria Gámez ([email protected]) 19 20 Keywords: species richness, carnivory, isotopes, niche breadth, rural, human footprint index, 21 mammal 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.19.423628; this version posted December 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. In review at Ecology Letters (December 2020) 22 23 Abstract 24 Predation is a fundamental ecological process that shapes communities and drives long- 25 term evolutionary dynamics. As the world rapidly urbanizes, it is critical to understand how the 26 built environment and other human perturbations alter predation across taxa. We conducted a 27 meta-analysis to quantify the effects of urban environments on three components of trophic 28 ecology in predators: dietary species richness (DSR), dietary evenness (DEV), and stable 29 isotopic ratios (δ13C and δ15N IR). We then evaluated whether intensity of anthropogenic 30 pressure, using the human footprint index (HFI), explained variation in the effect sizes of dietary 31 attributes using a meta-regression. We calculated Hedges’ g effect sizes from 44 studies 32 including 11,986 samples across 40 predatory species in 39 cities globally. The direction and 33 magnitude of effect sizes varied between predator taxonomic groups with reptile diets exhibiting 34 the most sensitivity to urbanization. Effect sizes revealed that predators in cities had comparable 35 DSR, DEV, and nitrogen ratios, though carbon consumption was significantly higher. We found 36 that HFI did not explain variation in effect sizes, a result consistent between the 1993 and 2009 37 editions of this metric. Our study provides the first assessment of how urbanization has perturbed 38 predator-prey interactions for multiple taxa at a global scale, revealing that the functional role of 39 predators is conserved in cities and urbanization does not inherently relax predation. 40 41 42 43 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.19.423628; this version posted December 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. In review at Ecology Letters (December 2020) 44 Introduction 45 Predation is a process which underpins ecological and evolutionary dynamics at various 46 scales, from the individual to the ecosystem. Predation can increase regional species richness 47 and diversity by mediating competition in prey species (Holt, 1977; Shurin, & Allen, 2001). 48 Moreover, predators alter ecosystem-level processes such as nutrient cycling by provisioning 49 carcasses and enriching soil or water columns (Schmitz et al., 2010). Apart from consumptive 50 effects, predation can structure communities indirectly through trophic cascades (Terborgh, 51 2010). The fear of predation itself can engender non-consumptive effects that alter space use and 52 aggregation of prey and subsequently drives vegetation patterns (Suraci et al., 2016; Gaynor et 53 al., 2019). While the theoretical and empirical literature is rich with studies quantifying the 54 effects of predation in natural systems, our understanding of how urban environments affect 55 predation remains limited, even contradictory. For example, predation rates on human landscapes 56 can be amplified by increased prey densities or relaxed due to an abundance of easily accessible 57 anthropogenic subsidies, creating an urban predation paradox (Rodewald et al., 2011; Fischer et 58 al., 2012). 59 Cities are an emerging socio-ecological ecosystem inducing novel interactions, 60 behavioral shifts, and evolutionary trajectories (Lowry et al., 2013; Johnson, & Munshi-South, 61 2017; Lepczyk et al., 2017). By 2030 more than 60% of the world’s human population is 62 projected to live in an urban area (United Nations, 2018). The effects on the landscape from such 63 rapid urbanization are profound; globally, urban land cover is projected to increase by 1.2 64 million km2 by 2030, decimating available habitat for wildlife and reducing agricultural land by 65 550,000 km2 (Seto et al., 2012; Bren D’amour et al., 2017). Urbanization can decrease prey 66 species richness and genetic diversity, alter community composition, and prey body size; thus, 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.19.423628; this version posted December 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. In review at Ecology Letters (December 2020) 67 altering resource availability and diet selection for secondary and tertiary consumers (El- 68 Sabaawi, 2018; Chejanovski, & Kolbe, 2019; Schmidt et al., 2020). Regional species pools are 69 further filtered by urban form and history, novel urban species interactions, and disparate 70 distributions of natural resources in the urban landscape due to systemic racism (Aronson et al., 71 2016; Schell et al., 2020). Additionally, human food subsidies increase trophic niche overlap in 72 terrestrial carnivores, potentially resulting in greater interspecific competition (Manlick, & Pauli, 73 2020). Cities also modify wildlife behavior, which influences vulnerability to predation or access 74 to food, by disrupting diel patterns and vigilance behaviors (Gaynor et al., 2018; Gallo et al., 75 2019). 76 Urbanization is a complex anthropogenic process that can alter predator-prey interactions 77 through a multitude of potential mechanisms associated with changes to food availability, habitat 78 connectivity, vegetation density, and microclimate (Alberti et al., 2020; Johnson et al., 2020). 79 Anthropogenic infrastructures bisect habitat, increase the cost and mortality risk of movement, 80 and create novel temperature gradients, driving changes to population and community-level 81 processes including predation (Golden, 2004; Fraser et al., 2019; Zambrano et al., 2019). Habitat 82 fragmentation can reduce prey abundance, affecting predator diet selection and evenness 83 (Layman et al., 2007). In particular, roads cause a significant proportion of wildlife mortality, 84 upwards of 49% of all adult and juvenile mortality for some species, and underlying the trend of 85 death rates exceeding birth and recruitment rates in urban areas (Bateman, & Fleming, 2012; 86 Tucker et al., 2018). In addition to fragmentation, extensive homogenization of urban vegetation 87 structure can reduce overall cover and affect prey behavior and space use (Denno, & Kaplan, 88 2007). 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.19.423628; this version posted December 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. In review at Ecology Letters (December 2020) 89 The effects of such varied mechanisms induced from urbanization manifest differently 90 among taxonomic groups with wildlife responses being scale-dependent (Fidino et al., 2020). For 91 example, cities exhibit extreme temperature gradients, which could result in varied consumptive 92 patterns, as low temperatures increased attack rate in Daphnia, while higher temperatures 93 increased the prey consumption rate in reptiles and birds (Wasserman et al., 2016; Scott et al., 94 2017). Herpetofauna are more susceptible to higher disease prevalence and toxicity in urbanized 95 ecosystems compared to mammal fauna (Murray et al., 2019). In some cases, urbanization can 96 even hamper the spread of disease as a result of reduced host densities in cities compared to rural 97 areas (Fountain-Jones et al., 2017; Gras et al., 2018). While patterns of species richness and 98 population density vary significantly across taxa, urban birds and arthropods tend towards 99 reduced diversity and increased abundance (Faeth et al., 2011; Mcdonald et al., 2020). 100 Despite the recent surge of urban ecology studies employing comparative urban vs. non- 101 urban frameworks, broad scale predation patterns across taxa remain largely unknown. Studies 102 often focus on a single species or city, limiting inference at a broad scale. Additionally, a lack of 103 a standardized definition of “urban” has made cross-city comparisons challenging, coupled with 104 varied experimental designs, sample sizes, and bias towards readily observable study organisms. 105 Thus, we lack a systemic understanding of how the urban environment affects predator diet, how 106 it varies across taxa, and how these effects scale with the intensity of human impact on the 107 landscape.
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