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Uq201d603 OA.Pdf 1 The mesoscavenger release hypothesis and implications for ecosystem 2 and human well-being 3 4 Christopher J. O’Bryan1,4,*, Matthew H. Holden2,3,4, and James E.M. Watson1,4,5 5 6 1School of Earth and Environmental Sciences, The University of Queensland, Brisbane QLD 4072, Australia 7 2ARC Centre of Excellence for Environmental Decisions, The University of Queensland, Brisbane, QLD 4072, 8 Australia 9 3Centre for Applications in Natural Resource Mathematics, School of Mathematics and Physics, The University 10 of Queensland, Brisbane, QLD 4072, Australia 11 4Centre for Biodiversity and Conservation Science, The University of Queensland, Brisbane, QLD 4072, 12 Australia 13 5Global Conservation Program, Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, New York, 14 USA 15 *Corresponding author 16 Christopher J. O’Bryan e-mail: [email protected] 17 Matthew H. Holden e-mail: [email protected] 18 James E.M. Watson e-mail: [email protected] 19 20 Keywords: scavenger, vulture, predator, cascade, dynamic model, conservation, human- 21 wildlife conflict, food webs, trophic level, top-down release 22 Article type: Ideas & Perspectives 23 Number of words in the abstract: 135 24 Number of words in the main text: ~3,800 25 Number of references: 58 26 Number of figures and tables: 4 Figures, 1 Table 27 28 Corresponding author full details: Address: Christopher J. O’Bryan, 8 Cottenham Street, 29 Fairfield QLD, Australia 4103. Phone: +61 449 599 035. E-mail: [email protected] 30 31 Data accessibility: no new data Author Manuscript 32 This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, 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/ELE.13288 This article is protected by copyright. All rights reserved 33 Statement of authorship: CO and JW conceived the idea of the manuscript. CO, MH, and 34 JW designed the research. CO conducted the literature review and wrote the manuscript. MH 35 developed the model. CO and MH modified the model, wrote model results, and developed 36 figures. 37 38 39 40 Abstract 41 Many apex scavenger species, including nearly all obligate scavengers, are in a state of rapid 42 decline and there is growing evidence these declines can drastically alter ecological food 43 webs. Our understanding of how apex scavengers regulate populations of mesoscavengers, 44 those less-efficient scavengers occupying mid-trophic levels, is improving; yet, there has 45 been no comprehensive evaluation of the evidence around the competitive release of these 46 species by the loss of apex scavengers. Here we present current evidence that supports the 47 mesoscavenger release hypothesis, the increase in mesoscavengers and increase in carrion in 48 the face of declining apex scavengers. We provide two models of scavenger dynamics to 49 demonstrate that the mesoscavenger release hypothesis is consistent with ecological theory. 50 We further examine the ecological and human well-being implications of apex scavenger 51 decline, including carrion removal and disease regulation services. 52 53 Introduction 54 Apex scavengers are functionally dominant at scavenging, meaning they can find and 55 consume carcasses more efficiently than other scavengers (Sebastián-González et al. 2016), 56 and can be either obligate or facultative scavengers. Obligate scavengers (i.e. Old and New 57 World vultures) are dependent entirely on carrion, but facultative scavengers rely partly on 58 carrion (Ogada et al. 2012a). Apex scavengers (i.e. vultures and functionally dominant 59 facultative scavengers) are facing unprecedented declines due to direct persecution, human 60 disturbance, collision with infrastructures and electrocution, poisons and other dietary toxins, 61 human disturbance, habitat loss and degradation, food shortage caused by sanitary 62 regulations, or abandonment of traditional farming practices (Ripple et al. 2014; Buechley & Author Manuscript 63 Şekercioğlu 2016). As such, it is imperative to understand the ecological and human well- 64 being impacts of apex scavenger declines (Buechley & Şekercioğlu 2016). There is growing 65 evidence of scavenger competitive release across Earth, where mid-sized, less efficient 66 scavengers (i.e., mesoscavengers) can increase in abundance in the absence of competition This article is protected by copyright. All rights reserved 67 from more efficient apex scavengers (the mesoscavenger release hypothesis; Figure 1) 68 (Butler & du Toit 2002; Sekercioğlu et al. 2004; Markandya et al. 2008; Ogada et al. 2012b; 69 Buechley & Şekercioğlu 2016; Morales-Reyes et al. 2017). The population effects of 70 mesoscavenger release from apex scavengers can be qualitatively similar to well documented 71 patterns observed in predatory systems, where the absence of apex predators releases 72 mesopredators (Crooks & Soulé 1999; Ritchie & Johnson 2009; Ripple et al. 2014; Newsome 73 et al. 2017). However, the mechanism behind mesoscavenger release is different; it is caused 74 by reduced competition over a shared resource, not the loss of top-down control. Here, we 75 present evidence pointing to the release of mesoscavengers by the loss of apex scavengers, 76 and we discuss potential ecosystem and human well-being implications of mesoscavenger 77 release. 78 79 Empirical support for the mesoscavenger release hypothesis 80 Mesoscavengers have been shown to be more abundant and diverse in areas that are absent of 81 apex scavengers (Table 1), which can affect ecosystem structure. For example, red foxes 82 (Vulpes vulpes), which are facultative mesoscavengers, were significantly more abundant in 83 areas of south-eastern Spain that lack vultures (Gyps spp.) compared to areas with vultures 84 (Morales-Reyes et al. 2017). Morales-Reyes and colleagues contend that mesoscavengers had 85 increased scavenging opportunities and thus consumed more carrion in the absence of 86 vultures, therefore resulting in increased abundance of foxes. An increase in mesoscavengers 87 has also been observed in India, where growing feral dog (Canis lupus) and rodent 88 populations have been linked to the widespread decline of vultures caused by ingestion of 89 veterinary pharmaceuticals (i.e. diclofenac) (Markandya et al. 2008). The authors suggest that 90 the concomitant rise of carrion without vultures resulted in a spike in mesoscavenger 91 populations (Markandya et al. 2008). In Tasmania, Australia, areas where Tasmanian devils 92 (Sarcophilus harrisii) have declined due to facial tumour disease have resulted in an 93 increased abundance of feral cats (Felis catus) and forest ravens (Corvus tasmanicus) 94 (Cunningham et al. 2018). The authors show that forest ravens have increased across all of 95 Tasmania during the period of Tasmanian devil decline. In areas of Spain and South Africa 96 where apex scavengers were lacking, species richness and composition drove the Author Manuscript 97 consumption of carrion; however, context-dependent effects (i.e. species abundance) had a 98 greater effect where apex scavengers were common (Mateo-Tomás et al. 2017). These apex 99 scavengers not only included globally widespread species such as wild boar (Sus scrofa), but 100 also imperilled species like gyps vultures (Gyps spp.) and African lions (Panthera leo) This article is protected by copyright. All rights reserved 101 (Mateo-Tomás et al. 2017). Likewise, in the Mendocino National Forest of California, foxes, 102 corvids, and rodents had significantly higher species richness at deer carcasses in the absence 103 of black bears and puma – the apex facultative scavenger and apex predator, respectively 104 (Allen et al. 2014). The authors argue that the nestedness, or structure of the scavenger 105 community, increased at carcasses where large carnivores were present (Allen et al. 2014). 106 107 In the absence of apex scavengers, mesoscavengers are thought to be less effective at locating 108 carrion, resulting in a longer carcass decomposition time. For instance, when turkey vultures 109 (Cathartes aura) and black vultures (Coragyps atratus) were experimentally excluded from 110 carrion in South Carolina, USA, 80 percent of carcasses were not scavenged by 111 mesoscavengers, resulting in a ten-fold increase in carrion that were not fully scavenged 112 compared to controls (Hill et al. 2018). A similar pattern was observed in Australia where 113 nearly 70 percent of carrion were not scavenged by mesoscavengers (rats, dogs, foxes, and 114 corvids) in the absence of apex facultative scavenging species such as kites (Haliastur spp.) 115 and white-bellied sea eagles (Haliaeetus leucogaster) (Huijbers et al. 2015). Similarly, 116 carrion persisted 2.6 times longer in areas where Tasmanian devils declined due to a facial 117 tumor disease (Cunningham et al. 2018). Carcasses were scavenged three times slower in the 118 absence of vultures in the Laikipia District of central Kenya (Ogada et al. 2012b) and thirteen 119 times slower in areas without vultures in south-eastern Spain (Morales-Reyes et al. 2017). 120 Not only are vultures more efficient at locating and consuming carrion in the Masai Mara 121 National Reserve in Kenya, they have also been shown to aid mesoscavengers in locating 122 carrion (Kane & Kendall 2017). As such, the loss of apex scavengers can result in increased 123 available carrion biomass and slower decomposition time likely due to
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