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Food for contagion: synthesis and future directions for studying host–parasite responses to resource shifts in anthropogenic environments

Sonia Altizer, Daniel J. Becker, Jonathan H. Epstein, Kristian M. Forbes, Thomas R. Gillespie, Richard J. Hall, Dana M. Hawley, Sonia M. Hernandez, Lynn B. Martin, Raina K. Plowright, Dara A. Satterfield, Daniel G. Streicker
Published 12 March 2018.DOI: 10.1098/rstb.2017.0102
Sonia Altizer
Odum School of Ecology, College of Veterinary Medicine, University of Georgia, Athens, GA, USACenter for the Ecology of Infectious Disease, College of Veterinary Medicine, University of Georgia, Athens, GA, USA
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  • ORCID record for Sonia Altizer
  • For correspondence: saltizer@uga.edu
Daniel J. Becker
Odum School of Ecology, College of Veterinary Medicine, University of Georgia, Athens, GA, USACenter for the Ecology of Infectious Disease, College of Veterinary Medicine, University of Georgia, Athens, GA, USADepartment of Microbiology and Immunology, Montana State University, Bozeman, MT, USA
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Jonathan H. Epstein
EcoHealth Alliance, New York, NY, USA
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Kristian M. Forbes
Department of Virology, University of Helsinki, Helsinki, FinlandDepartment of Biology, The Pennsylvania State University, University Park, PA, USACenter for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA, USA
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  • ORCID record for Kristian M. Forbes
Thomas R. Gillespie
Department of Environmental Sciences and Program in Population Biology, Ecology and Evolution, Rollins School of Public Health, Emory University, Atlanta, GA, USADepartment of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, GA, USA
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Richard J. Hall
Odum School of Ecology, College of Veterinary Medicine, University of Georgia, Athens, GA, USACenter for the Ecology of Infectious Disease, College of Veterinary Medicine, University of Georgia, Athens, GA, USADepartment of Infectious Disease, College of Veterinary Medicine, College of Veterinary Medicine, University of Georgia, Athens, GA, USA
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Dana M. Hawley
Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA
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Sonia M. Hernandez
Warnell School of Forestry and Natural Resources, College of Veterinary Medicine, University of Georgia, Athens, GA, USASoutheastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA, USA
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Lynn B. Martin
Department of Integrative Biology, University of South Florida, Tampa, FL, USA
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Raina K. Plowright
Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA
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Dara A. Satterfield
Migratory Bird Center, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20008, USA
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Daniel G. Streicker
Odum School of Ecology, College of Veterinary Medicine, University of Georgia, Athens, GA, USAInstitute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow G12 8QQ, UKMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK
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Abstract

Human-provided resource subsidies for wildlife are diverse, common and have profound consequences for wildlife–pathogen interactions, as demonstrated by papers in this themed issue spanning empirical, theoretical and management perspectives from a range of study systems. Contributions cut across scales of organization, from the within-host dynamics of immune function, to population-level impacts on parasite transmission, to landscape- and regional-scale patterns of infection. In this concluding paper, we identify common threads and key findings from author contributions, including the consequences of resource subsidies for (i) host immunity; (ii) animal aggregation and contact rates; (iii) host movement and landscape-level infection patterns; and (iv) interspecific contacts and cross-species transmission. Exciting avenues for future work include studies that integrate mechanistic modelling and empirical approaches to better explore cross-scale processes, and experimental manipulations of food resources to quantify host and pathogen responses. Work is also needed to examine evolutionary responses to provisioning, and ask how diet-altered changes to the host microbiome influence infection processes. Given the massive public health and conservation implications of anthropogenic resource shifts, we end by underscoring the need for practical recommendations to manage supplemental feeding practices, limit human–wildlife conflicts over shared food resources and reduce cross-species transmission risks, including to humans.

This article is part of the theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.

1. Introduction

Human feeding of wildlife is pervasive and can occur through both intentional (bird feeders, tourist sites; [1,2]) and unintentional routes (landfills, agricultural crops; [3,4]). In response, animal populations can shift movement behaviours or geographic ranges, experience higher densities and contact rates and show changes in demographic rates and interactions with other species. The population- and community-ecological consequences of supplemental feeding in wildlife have rarely been explored and could be far-reaching, particularly for infectious disease dynamics [5–8].

Papers in this issue directly examine the interactions between anthropogenic resource subsidy and infectious disease dynamics in wildlife using diverse approaches that include mechanistic models, observational field studies and experiments, analysis of citizen science data, and synthetic reviews. Empirical studies presented here examine diverse and engaging empirical systems, ranging from birds at backyard feeders, to bats in urban and agricultural environments, to elk in Yellowstone National Park (figure 1). Despite differences in the biology of distinct systems and environmental contexts, papers in this theme issue point to common questions, patterns and challenges for future work. Our goals in writing this synthesis are to identify these common threads and outline several immediate priorities for future research on the links between human resource subsidies and wildlife disease.

Figure 1.
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Figure 1.

Taxonomic breadth of hosts provisioned by humans covered by studies in this theme issue: (a) common vampire bat (Desmodus rotundus) in Belize (Brock Fenton), (b) elk (Cervus elaphus) in the Greater Yellowstone Ecosystem (Paul Cross), (c) monarch butterflies (Danaus plexippus) in Mexico (Natalie Tarpein), (d) house finch (Haemorhous mexicanus) infected with Mycoplasma gallisepticum in North America (Bob Vuxinic), and (e) Daphnia dentifera infected with a fungal pathogen (Metschnikowia bicuspidata) (Tad Dallas [9]).

The taxonomic breadth of hosts and pathogens affected by resource provisioning, and the range of food sources examined here, underscore how pervasive this phenomenon has become. Given that responses of several pathogens studied here are accompanied by elevated risks of cross-species transmission to humans, livestock or vulnerable wildlife populations, studies that provide a mechanistic understanding are sorely needed to predict future responses to feeding by humans. The inevitability that human populations will continue to expand, alter habitats globally and encroach on wildlife, means that animal use of resources provided by humans will only increase, lending a sense of urgency to understanding the impacts for wildlife, domestic animal and human health [10].

2. Key findings and common threads across diverse systems and approaches

(a) Host immunity shows complex responses to resource provisioning

Because mounting and maintaining immune defences require energy and nutrients [11,12], access to anthropogenic food subsidies could increase the immune function of wildlife, especially during times or in habitats where natural food sources are scarce or limited [13]. Under the common assumption that provisioning leads to better-defended hosts, pathogen transmission should decrease owing to lower infection probability or faster recovery times [14,15], but such effects might be offset by other processes like aggregation around food that increase pathogen transmission [16]. Hite & Cressler [17] used a nested mechanistic models to show that even if resources decrease host susceptibility to infection, an increase in host densities in response to resource subsidies can override this effect and produce a higher total transmission rate.

Empirical studies in this issue showed that the relationship between provisioning and immunity can depend on the type of defence, quality of resources, and host and pathogen taxonomy, leading to divergent outcomes among study systems (reviewed in Strandin et al. [18]). This finding is consistent with past work on domesticated animals showing that different components of host immunity respond differently to resource subsidies, in part because of the variable costs of different immune process, and also because key macro- and micronutrients can lead to immune system biases [19,20]. In natural systems, Becker et al. [21] found that abundant livestock as food for vampire bats predicts stronger innate immunity relative to adaptive immunity. Heightened innate immunity in the bats was further associated with a lower probability of infection by Bartonella and haemoplasmas. Importantly, individual dietary history itself did not strongly predict variation in bat immune profiles, suggesting that broader habitat-level factors associated with livestock rearing could underlie parasite exposure and host immunity. In other cases, such as elk supplemented at winter feedgrounds (Cotterill et al. [22] and urban flying foxes [23], researchers hypothesized decreased immunocompetence with food provisioning, owing to elevated stress hormones stemming from high host densities and due to coinfections that impair immune response. Immune activity can also be compromised if human-provided food is contaminated with toxins or drugs. As a case in point, Spanish imperial eagles supplemented for conservation purposes with domestic rabbits (that had been treated with antibiotics and antiparasitic drugs) showed decreased complement activity owing to the presence of pharmaceuticals (especially fluoroquinolones) in their food [24]. Similarly, vampire bats that fed more consistently on domestic animals in agricultural habitats had higher concentrations of mercury that were associated with weaker bacterial killing ability of plasma [25].

It is important to note that evidence for nutritional condition altering wildlife immune defences is limited to a relatively small number of hosts, and studies of macro- and micro-nutrient influences on immunity are needed to more critically evaluate this assumption. Genome-wide RNA sequencing could help researchers focus on particular defence mechanisms by quantifying immune gene expression between provisioned and unprovisioned groups, and those with or without known infections [26,27]. In future work, phylogenetically informed meta-analysis could help quantify the importance of food quantity, quality, and host and pathogen traits [28] for immune defence and infection outcomes across wildlife systems.

(b) Behavioural changes in foraging and contact can alter local transmission processes

Several studies in this theme issue demonstrate how resource provisioning can alter key behaviours that underlie pathogen transmission, including foraging behaviour, aggregation and contacts between species [16,29,30]. Crowding of individuals around supplemental resources can lead to higher host densities and contact rates, and thus increase density-dependent transmission, as illustrated previously through theoretical models [14]. Moyers et al. [31] designed an experiment to test how feeder density influenced contact rates and exposure to the bacterium Mycoplasma gallisepticum in captive house finches. Their work showed that higher bird feeder density in enclosures caused the rapid spread of clinical infections, whereas lower feeder density reduced pathogen spread, possibly due in part to the presence of sub-clinical and potentially immunizing exposures. Importantly, further work is needed to examine how individual-level host heterogeneity in the use of supplemental resources contributes to population-level infection dynamics. For example, can subsets of hosts that aggregate around resources act as super-spreaders, or might host heterogeneity limit the population-level spread of disease?

Cotterill et al. [22] reviewed the implications of intentional winter feeding of elk (to limit encounters with cattle) in the western USA. Feed grounds have facilitated brucellosis transmission among elk by elevating local density and contact rates [32] and, more speculatively, by decreasing immune function. Feeding has now created a policy conundrum: high infection prevalence in elk leads to greater motivation to separate elk and cattle, which leads to continued winter feeding and further infection risk. While numerous papers in this theme issue advance a mechanistic understanding of the links between disease and provisioning, disentangling the roles of aggregation and subsequent contact rates, versus changes in immune functions, for driving pathogen transmission will require further work.

Resource provisioning often causes changes in diet and foraging behaviours, especially among urbanized wildlife populations that subsist on supplemental food. Murray et al. [33] showed that white ibises shifting from natural wetlands to urban parks in Florida, where they commonly forage on provisioned food, have lower ectoparasite burdens. To explain this pattern, the authors hypothesize that easier food access might allow birds to spend less time foraging and more time preening to remove parasites. In urban and coastal Queensland, the Australian white ibis experienced explosive population growth in the 1990s due to provisioning from open landfills [34,35]. The abundance of anthropogenic food waste and deliberate feeding in urban parks led to a shift from coastal nesting and foraging to suburban and urban foraging, bringing ibis into greater contact with each other, and with chickens on poultry farms and people in recreational areas [34]. Increased population density and interaction among ibis and with domesticated animals and people could also increase the risk of intra- and interspecies pathogen transmission. Understanding the mechanistic links between shifts in behaviour and disease risk could be strengthened by future studies that simultaneously measure specific behaviours (at the individual level) and changes in infection (at individual and population levels). For some food-provisioned populations, efforts to limit contact rates during high-risk intervals (e.g. by ending feed dates earlier in the season for elk, or spacing out bird feeders at lower density) or preserve particular behaviours (e.g. such as preening or other anti-parasite behaviours) could prove important for managing infection risk in wildlife.

(c) Behavioural changes in host movement can influence landscape-level disease processes

Provisioning can cause changes to host movements and infection patterns at large spatial scales. As reviewed by Satterfield et al. [36], anthropogenic food subsidies can decrease migratory movements and concentrate hosts into resource-subsidized regions, where greater host aggregation, year-round parasite accumulation and longer residency times could increase exposure to pathogens [6,28]. The authors note that shifts towards more sedentary behaviour in response to resource provisioning have occurred for multiple migratory and nomadic species, in some cases associated with resulting increases in infection risk [37–40]. For example, satellite telemetry studies of Pteropus medius, the reservoir for Nipah virus in Bangladesh, suggest that this species is much more sedentary than its relative, P. vampyrus in Malaysia, which could be due, in part, to anthropogenic food resources (Epstein et al., unpublished) [41]. Date palm sap, harvested by humans in Bangladesh, is exploited by frugivorous bats throughout the winter months and is the primary route of Nipah virus spillover from bats to people [42,43]. Alternatively, animals that stop migrating might be exposed to a lower diversity of parasites across their migratory range, and more limited host movements could reduce the spatial spread of pathogens [44,45]. A theoretical model [46] explored these questions for a partially migratory host affected by a vector-borne pathogen. The model showed that when provisioning increased the survival of resident hosts during the non-breeding season, both infection prevalence and the fraction of the population that is non-migratory increased. Because greater proportions of residents permit the sustained transmission of pathogens, this behavioural shift could be especially costly to remaining migrants that travel through areas with infected residents; resource provisioning could therefore threaten the persistence of migratory behaviour.

For some highly mobile hosts, resource provisioning will alter daily foraging movements and habitat use. In Australia, naturally nomadic fruit bats have shifted into urban areas where they feed on native and exotic flowering and fruiting trees planted by humans [38,47]. Paez et al. [48] applied optimal foraging theory to explore how urban bat colonies alter their foraging strategies in response to decreasing native habitat and seasonal food availability. Their work predicts that residency in urban patches will increase as native foraging habitats become more isolated, and during periods of overall food scarcity. Longer residency in urban centres could set the stage for less frequent but larger viral outbreaks in bats, resulting in higher exposure to humans and domesticated animals [47,49].

(d) Changes to interspecific interactions can cause cross-species transmission and pathogen emergence

Cross-species pathogen transmission requires several ecological, epidemiological and behavioural factors to align [50]. Importantly, anthropogenic provisioning can influence multiple components of this alignment by (i) changing host community composition, (ii) altering infection dynamics within populations of reservoir hosts, and (iii) affecting contact rates between host species. First, because the responses of host species to novel resources in human-altered landscapes can range from disappearance to explosive population growth, provisioning can dramatically alter host community composition and patterns of pathogen transmission [51–53]. As an example of these changes, large-scale monocultures in Brazil and Panama altered rodent communities and increased human exposures to rodent species infected with hantavirus [54,55]. At the largest spatial scales, provisioning could expand host geographic ranges, creating novel opportunities for cross-species transmission where hosts previously did not co-occur [56]. Second, changes to infection dynamics within primary host species (see above sections) can have knock-on effects that amplify or dampen the probability of transmission given interspecific contacts [16]. Third, even if host community composition and disease dynamics in reservoir species remain unchanged, provisioning can facilitate cross-species transmission by altering the frequency and nature of interspecies contacts. For example, bats foraging on mango trees planted near pig farms, or bats drinking palm sap as it runs down tree trunks into collecting vessels, created new routes of Nipah virus transmission from bats to pigs and humans, respectively [43,57]. The common practice of allowing domestic animals to feed on dropped or bitten fruit, that may have been contaminated by bats, also increases the risk of pathogen transmission [58,59]. In Bangladesh, 26 common fruits grown and eaten by people are known to be eaten by frugivorous bats, and eating dropped fruit with animal bite marks regularly occurs (Epstein et al., unpublished.) Similar processes could influence pathogen transmission among wildlife when resources promote multi-species aggregations of previously ecologically isolated species [60,61]. Importantly, these mechanisms of resource-driven changes in cross-species transmission might act synergistically. As discussed by Becker et al. [21], livestock both stimulates vampire bat population growth and, by its own presence, expands opportunities for cross-species transmission of rabies virus and potentially other pathogens.

Altered dynamics of cross-species transmission are among the most visible and alarming responses to resource provisioning because they can directly impact human health, agriculture, or the conservation of vulnerable wildlife populations. For example, livestock-driven increases in vampire bat rabies have made this disease one of the three most important zoonoses in Latin America and a significant barrier to the advancement of agrarian communities [62,63]. Similarly, the resource-driven rise of Hendra virus cases in humans and horses in Australia created economic and social challenges, ranging from the rising need for veterinary vaccines to protect horses, to conservation challenges as bat persecution is promoted for disease control [47,64]. In Asia, the transmission of zoonoses from provisioned non-human primates to people impacts tourism [65]. Importantly, provisioned landscapes can provide opportunities for spillover infections from humans (or livestock) to wildlife, and potential spillback into humans. For example, in parts of Africa, baboons commonly frequent human settlements and obtain food from houses or waste sites. Parasitological surveys showed baboons near these settlements can harbour parasitic worms and protozoa that commonly infect humans, although further diagnostic work is needed to determine whether the primate isolates match parasite genotypes recovered from nearby humans [66,67]. Better quantifying the contexts under which provisioning mediates cross-species transmission could provide an epidemiological lever to promote more responsible management of anthropogenic food subsidies for wildlife.

3. Critical priorities for future work

(a) Taxonomic biases in studies of provisioning and infection

Work included in this Theme Issue reflects the taxonomic breadth of hosts and parasites studied in the context of resource provisioning, and also highlights taxonomic gaps to be addressed in future work. The empirical studies presented here focus primarily on mammals (e.g. bats, ungulates) and birds (e.g. passerines, wading birds), with less representation from invertebrates (e.g. monarch butterflies, Daphnia). Studies here also focused heavily on microparasites, particularly bacteria and viruses, transmitted through direct and non-close contact (e.g. faecal–oral routes), although ectoparasites are also represented. More generally, throughout the literature, studies of provisioning and host–parasite interactions are biased towards these taxa (reviewed in [16,28]). For example, a recent meta-analysis of over 300 host-parasite interactions was dominated by studies of microparasites transmitted by close and non-close contact, and of helminths transmitted through non-close contact and intermediate hosts [28]. Vector-borne diseases, and protozoan and fungal parasites are generally poorly represented, highlighting a priority for future studies, particularly in light of expanding vector distributions under climate change and the role of fungal parasites in wildlife population declines [68–71]. Past studies of food provisioning and wildlife disease are also heavily biased towards mammals and birds, with much less work on invertebrates and other ectotherms. Civitello et al. [72] highlight how nutrient inputs into aquatic ecosystems (as a form of anthropogenic subsidy) can have similar effects on host-parasite interactions as food subsidy to wildlife (by increasing host density and altering parasite production within hosts). This observation stresses the need for greater inclusion of amphibians, reptiles, fish, and invertebrates in studies of provisioning and disease.

(b) Modelling studies to link effects of provisioning across biological scales

Resources can affect within-host processes relevant to pathogen colonization, between-host transmission at the population level, and landscape-level processes such as host dispersal. Mathematical models provide powerful tools for linking infection dynamics across scales of organization and for informing the conditions under which provisioning can increase or decrease infection. For example, theory to date has shown that when resources strongly enhance host defences, this can limit pathogen transmission that otherwise would increase from resource-induced increases in host density [14,73]. If host defences are unchanged or weakened by human-provided resources, increased exposure to pathogens resulting from elevated host densities and behavioural changes are likely to increase pathogen invasion and prevalence [16]. A separate body of theory used metapopulation models to examine how the distribution of resource-rich habitats, and their impact on colonization and extinction, affects host–pathogen dynamics. This work shows that increasing the frequency of provisioning across the landscape increases pathogen establishment and spread; yet nonlinear relationships between infection prevalence and the relative abundance of provisioned habitats can emerge if provisioning and infection influence host movement decisions and dispersal success [74,75]. Despite these recent advances, a need remains for mathematical models that more explicitly link processes across individual, population, and landscape scales.

In this issue, Hite & Cressler [17] contribute a cross-scale approach by developing a mechanistic framework coupling within-host processes (through improved immune defence and increased pathogen replication in response to resources) and between-host processes (through transmission and resource-mediated population growth rates). Their model explores the consequences of resource acquisition for parasite virulence evolution and its potential to stabilize resource-driven cycles in host population dynamics. The authors demonstrate that linking within-host and population-level processes can produce cyclic host population dynamics and associated within-host cycles of high and low parasite replication, an emergent phenomenon that does not occur when within-host processes are ignored. In other work, Civitello et al. [72] demonstrate that incorporating trophic complexity (by considering predators and competitors of provisioned hosts) can reverse predictions about resource-mediated increases in pathogen prevalence. Resource subsidies increase pathogen prevalence when only hosts are present, but competitors and predators can lower infection prevalence (in some cases causing pathogen extinction) when resources are abundant. These studies highlight the importance of considering processes at scales above and below the population level in predicting resource subsidy effects on pathogen transmission dynamics. An additional key insight from theoretical work is that empirical studies must be long enough relative to the duration of infection to capture stable or cyclic responses of population and infection dynamics under provisioning. Promising future avenues include investigating how resources affect coinfection (e.g. in shaping immune-mediated competitive interactions between micro- and macroparasites); the responses of parasites with complex transmission modes (e.g. vector-borne and trophically transmitted parasites); and relationships for multi-host pathogens where host species that differ in competence might respond differently to provisioned resources (e.g. in population density or susceptibility to infection) [10].

Future theoretical models that are paired closely with detailed empirical work could be especially fruitful in understanding the dynamical outcomes of provisioning. Such work could couple local and landscape-level effects of resources on well studied host–pathogen interactions. Given that theory to date on provisioning and infection has focused separately on population and metapopulation scales, one area that is crucially needed involves models that explicitly link local dynamics (e.g. resource effects on individual hosts or contact rates) to regional movements of the host and pathogen that also depend on resource distributions (figure 2). From an applied perspective, such models could also allow researchers to predict the outcomes of different habitat management scenarios that might alter resources in ways that lower infection risks [14,74,76].

Figure 2.
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Figure 2.

Interactions between human-provided food and pathogen dynamics can occur at multiple scales of organization, as illustrated by American white ibis (Eudocimus albus) and environmentally transmitted enteric pathogens. Anthropogenic food subsidies in urban habitats could influence within-host dynamics (e.g. individual susceptibility and intensity of pathogen shedding, on left), local transmission processes (e.g. intra- and interspecific contact rates, uptake of pathogen from the environment, in centre) and landscape dynamics (e.g. host movement between natural and provisioned habitats, site fidelity, on right). Combined modelling and empirical work is needed to quantify the importance of processes operating within scales, and to predict how processes at one scale affect dynamics at larger scales of organization. (Online version in colour.)

(c) Experimental manipulations of food resources to quantify responses of hosts and pathogens

Research manipulating food resources is noticeably rare among the growing body of literature developing around the effects of anthropogenic food subsidies on host–parasite dynamics. Indeed, this theme issue reflects this disparity between observational and experimental approaches, with only a single study [31] among the latter. A handful of studies published elsewhere have experimentally manipulated food; for example, work by Wright & Gompper [77] showed that clumped food resources increased the transmission of endoparasites in raccoons, suggesting a possible behavioural mechanism for changes in prevalence. Wilcoxen et al. [78] and Galbraith et al. [79] both manipulated the presence or absence of bird feeders and found effects of feeder presence on health-associated traits such as body condition, as well as effects on the prevalence of diverse parasites and pathogens. Responses to feeder presence in Galbraith et al. [79] were parasite- and host-specific. Although experimental in nature, field studies such as these still have difficulty establishing definite causation (e.g. in contrast, see [80]). For example, in some systems, diseased animals could be more strongly motivated to seek out supplemental food resources, leading to patterns of higher infection prevalence at supplemented sites that could also be interpreted as a positive effect of resources on pathogen transmission [81].

Most experiments to date manipulate food through experimental supplementation, but future work could reduce access to anthropogenic foods, especially for species for which finding or monitoring unprovisioned populations is difficult. For example, vampire bats in Latin America are most abundant and thus readily sampled near livestock-rich areas [82], and locating unprovisioned rainforest populations is difficult [83]. Moreover, multiple confounding factors, including habitat characteristics and host density, differ between provisioned and unprovisioned groups [21]. In this case, restricting access to livestock, such as through artificial lighting to deter bat feeding [84], might be one way to monitor host and pathogen responses to reduced access to anthropogenic food. For other hosts, limiting access to human foods through fencing, or through campaigns to restrict tourist feeding of wildlife, could generate heterogeneity in resources.

Manipulating food quantity and quality is needed to explore the effects of food nutritional value on multiple measures of host immune defence, the host microbiome (discussed below), and susceptibility to target pathogens. Some experimental provisioning work has examined individual and population-level outcomes in birds and rodents [85–88]. Many of these experiments have been conducted in semi-controlled settings, such as aviaries and field enclosures, reflecting challenges associated with regulating food and disease exposure in free-ranging wildlife, which can disperse over large areas. However, confinement might also impact disease outcomes in unnatural ways, such as by increasing the frequency and intensity of intraspecific transmission opportunities, and inducing stress that often impairs host immunity [18].

Future field experiments might simultaneously control multiple components of provisioning, especially if anthropogenic foods dampen the seasonality or pulsed timing of natural resources, and at the same time make food more spatially aggregated, or change resource quality. These same studies could experimentally reduce infections in some hosts, to separate responses of host behaviour, physiology and fitness from parasite infection itself. Given the pervasiveness of provisioning, many opportunities exist to integrate experiments within current feeding activities, particularly within wildlife management and conservation efforts (e.g. [22]). Moreover, the strong causal inference provided by well-planned and executed experiments (e.g. by manipulating both infection and resources in free-ranging wildlife [85]) necessitates greater emphasis on these approaches to better understand how anthropogenic resources affect host–parasite dynamics.

(d) Understanding consequences of resource subsidies for the evolution of pathogen virulence

By affecting pathogen transmission and within-host processes, resource provisioning could ultimately affect host and pathogen evolution, an idea explored in depth by Hite & Cressler [17]. General theory on virulence evolution predicts that greater opportunities for horizontal pathogen transmission, such as might be created by aggregation around provisioned resources, could favour the evolution of more virulent pathogen strains [89]. As described earlier, Hite & Cressler's paper used a multi-scale model to show that such a result can arise even when provisioning increases host immunity. Empirical work is crucially needed from naturally occurring host–pathogen systems to test the virulence of pathogen strains from provisioned and unprovisioned host populations (e.g. [37]).

Although not examined by papers in this issue, provisioning can, in some cases, allow wildlife to better tolerate infection [16], an idea supported by laboratory studies demonstrating that improved nutrition can prolong the survival of infected animals and increase the duration of pathogen shedding [90,91]. Because host mortality cuts short the infectious period for many pathogens, this can constrain greater within-host replication by pathogens, and hence limit virulence evolution. By contrast, more tolerant hosts could select for more virulent pathogen strains by releasing pathogens from some of the costs of virulence [90]. Thus, although improved condition could reduce disease-induced mortality of provisioned hosts in the short term, provisioning could favour the evolution of higher virulence in the longer term [92]. Evolutionary models and empirical studies that explore the impact of resource subsidies on host tolerance to infection, within the context of other processes, are needed to identify the conditions under which provisioned populations support pathogen strains of higher virulence.

(e) Seeking how changes to the host microbiome affect larger-scale infection processes

Another important area for future work is understanding how dietary changes associated with provisioning could impact the host microbiome and within-host dynamics [16]. The composition of gut microbial communities can influence the immune system, thereby affecting host susceptibility and pathogen colonization [93]. For example, experimental simplification of microbiota from Cuban tree frog tadpoles increased their susceptibility to invasion by gut helminths as adults [94]. The composition and diversity of the gut microbiome is itself strongly shaped by individual diet [95,96], and thus provisioned wildlife would be expected to differ in both their microbiota and their susceptibility to enteric pathogens. Yet field studies of microbiomes in provisioned hosts are rare; in one example, the gut microbiota of baboons foraging on leftover food in Bedouin settlements mirrored the gut microbiota of people living in the Bedouin communities [97].

Comparative work on the microbiome between provisioned and wild populations is necessary to establish how specific dietary differences influence gut microbial composition and diversity. For example, shifts from protein- to carbohydrate-rich diets in urban-foraging wildlife such as white ibis [33] could have especially pronounced effects on microbiomes, and, in turn, pathogen invasion. In one rare case study, shifts toward grain-based diets may have disrupted the microbiota of Canada geese and facilitated Clostridium perfringens colonization [98]. From another perspective, foraging on anthropogenic resources in urban and agricultural environments could also expose species such as vampire bats and flying foxes [21,48] to contaminants (e.g. pesticides and antibiotics) that alter microbial community composition [99]. When possible, manipulative experiments are needed to examine causal relationships between different components of provisioned diets and the microbiome. Moreover, relationships among microbiome diversity, microbiome composition and susceptibility to pathogen challenge in the context of provisioning must be elucidated to understand how changing microbiota influences host susceptibility to infection. Finally, data linking diet, microbial diversity and immunity could be used to parameterize mathematical models to holistically explore how provisioning influences infection dynamics.

4. Implications of provisioning for conservation and human health

(a) The importance of understanding human motivations for feeding wildlife

The pervasiveness and popularity of intentional wildlife provisioning (e.g. [100]) suggests that humans have strong underlying motivations for this activity, particularly in the case of backyard bird feeding, on which people spend $4.5 billion annually in the USA alone [101]. Although bird feeding is the most prevalent form of intentional provisioning, a clear picture of the disease risks this activity imposes on wildlife and humans remains elusive [81]. The intentional feeding of charismatic mammals is common and probably alters disease risk as well. For example, provisioning of wild primates is prevalent within the context of Hindu and Buddhist culture, and has been enhanced with increasing tourism [102]. Motivations for feeding wildlife are complex and may vary regionally [103,104], but numerous studies have shown a key impetus of the psychological benefits of direct human–wildlife interaction [105], including a sense of pleasure or relaxation, feelings of usefulness and an increased connection to nature [106–109]. In fact, the vast majority of people surveyed about their willingness to interact with wild primates were aware of the potential disease risks associated with this interaction, and yet more than half still responded that they would touch wild primates if given the opportunity [110]. Welfare motivations are also commonly cited by those who provision wildlife [108], including a desire to help wildlife or ‘assist them through hard times' [107,109]. Indeed, provisioning tends to be strongest in seasons when natural food is perceived to be limited [107], suggesting a strong role of welfare motivations.

Cox & Gaston [100] suggest that positive reactions from wildlife, as well as psychological benefits to humans, strongly motivate people to offer supplemental foods, although more empirical evidence is needed. For example, humans that receive significant positive benefits from feeding (increased well-being or reduced stress) are probably more likely to continue provisioning. On the other hand, Cox & Gaston [100] also propose that the negative consequences of supplemental feeding, such as disease transmission among wildlife [111], or human health risks, often do not feed back to dampen provisioning behaviour because these effects are rarely apparent to the public [107]. The recent trend toward reduced feeding of (non-bird) wildlife in the USA [100] suggests that active campaigns against feeding of mammals are beginning to influence human behaviour. Thus, by tapping into the welfare motivations for feeding wildlife, changes in human behaviour are possible. Success in changing behaviour might be more even more likely when campaigns directly target the negative effects on humans, such as in cases of human–wildlife conflict and pathogen spillover.

To the extent possible, intentional supplemental feeding should be managed to maximize benefits to both humans and wildlife. For example, the recently documented association between higher levels of afternoon bird abundance and reductions in the severity of depression, anxiety and stress in humans led the authors to propose the active use of supplemental feeding to create ‘optimal’ bird abundance levels for human health [112]. For many bird species, supplemental feeding decreases starvation risk [113] and can improve breeding success [114]. Yet, feeding has also been associated with changes in community structure [115], range expansion [116], and, as this issue illustrates, pathogen transmission. Unfortunately, it seems unlikely that optimal levels of feeding for humans and wildlife will coincide. Thus, given the species- and habitat-specific effects of supplemental feeding [115,117], determining the ideal levels of provisioning for most wildlife will be challenging. In cases where clear negative effects of resource provisioning on wildlife are documented, educational campaigns would ideally leverage welfare-driven motivations for feeding by creating negative feedback loops on human behaviour [100]. Overall, effective management of intentional provisioning will require significantly more data than are currently available on both human motivations for feeding, effects of feeding on wildlife and potential feedback loops between wildlife effects and human behaviour. Given the enormous and potentially growing scale of human supplementation of wildlife [101], developing effective management tools is both timely and critical.

(b) Recommendations for limiting disease risks associated with human–wildlife contacts

The proximity with wildlife afforded by resource subsidies in urban and agricultural landscapes brings humans and domestic animals into contact with wildlife pathogens, and wildlife into contact with human pathogens (figure 3). Some of the most readily observed examples include growing populations of urban mesocarnivores (e.g. foxes, raccoons and skunks) that can attack humans and domestic animals when infected with rabies [118]. Non-human primates can also become aggressive following habituation to human-provided food, leading to the transmission of zoonotic viruses in some cases [119], and exposing primates to respiratory infections from human researchers and tourists in other scenarios [120]. Wildlife professionals might be exposed to zoonotic pathogens when translocating non-human primates in response to human–wildlife conflict [121]. Even when interspecific contacts between wildlife and humans are rare, pathogens can transfer between humans and wildlife by environmental routes or through arthropod vectors. Examples include a rise in human infections with the soil-borne tapeworm Echinococcus multilocularis, attributed to provisioned urban red foxes in Europe [122]. Human and animal Nipah virus infections have occurred through the consumption of food contaminated by bat excreta [123,124], and greater human exposures to hantavirus through environmental infectious stages followed the growth of rodent populations that exploit agricultural crops [54,55]. Zooanthroponoses (pathogens transmitted from humans to other animals) are less appreciated, but affect wildlife globally [125,126]. The preponderance of environmentally and vector-transmitted pathogens at the human–wildlife interface raises important challenges to recognize links with resource provisioning. Epidemiological investigations that identify agents of disease must be followed with ecological studies to identify natural hosts and the ecological context that enables cross-species transmission [127]. Fortunately, rapid and powerful DNA/RNA sequencing technologies [128], together with increasingly sophisticated tools for inferring pathogen transmission between species [129] offer currently under-used opportunities to improve scientific understanding of the changing patterns of pathogen transmission in provisioned environments.

Figure 3.
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Figure 3.

Possible effects of provisioning on amplifying pathogen spillover risks by (1) increasing pathogen transmission and shedding from reservoir hosts (e.g. through increased aggregation, susceptibility and shedding intensity) and (2) increasing opportunities for contact between humans and domestic animals and either reservoir hosts or pathogen in the environment. Silhouettes and arrows display case studies from this theme issue where provisioning had little effect or decreased infection relative to more natural environments (black; white ibis, vampire bats) and where provisioning amplified infection cycles (red; flying foxes, elk, house finches) and could potentially increase the risks of cross-species transmission.

Under some circumstances, ecological interventions that build on a mechanistic understanding of host and pathogen biology can prevent cross-species transmission. Most notably, preventing wildlife access to unintentionally provisioned resources, or creating a barrier between provisioned resources and domesticated animals (e.g. planting orchards away from livestock enclosures to reduce the risk of Nipah spillover on farms in Malaysia), can restrict opportunities for overlap between host species and function as a barrier to pathogen spillover [50]. As one key example, blocking the foodborne transmission of Nipah virus from pteropid fruit bats to humans using a bamboo skirt placed at the top of date palm sap collection pots restricts bat access to this shared food resource, and could reduce the risk of Nipah virus exposure in humans [130,131]. This case study highlights not only how basic ecological data on the foraging behaviour of reservoir hosts can aid in the design of interventions, but also how insights from social science and the application of locally available practices can produce economically affordable management tools [132]. Such ‘ecological interventions' may also be cheaper and more effective than antibiotics or vaccines that are mobilized after cross-species exposures occur. Other intervention strategies can promote sanitary best practices to prevent the build-up on infectious stages on feeders (e.g. washing backyard bird feeders), encouraging the dispersal of feed in smaller units over larger areas to reduce aggregation and lower contact rates (e.g. with management-based feeding [133]), and educating the public about disease risks posed by well-intentioned but harmful feeding activities [134,135]. Given that resource provisioning is ultimately derived from human actions, perceptions and policies, the integration of ecological, sociological and management perspectives will be a key lever by which infectious disease risks can be minimized for the well-being of humans, domesticated animals and wildlife.

Data accessibility

This article has no additional data.

Authors' contributions

S.A. and D.J.B. developed and organized the paper, drafted sections of the paper, integrated author contributions and created associated figures. All other authors participated in the design of the paper, drafted sections of the manuscript and helped revise the paper. All authors gave final approval for publication.

Competing interests

We declare we have no competing interests.

Funding

Authors were supported by grants from the National Science Foundation: NSF DEB-1518611 (S.M.H., R.J.H., S.A.), NSF DEB-1601052 (D.J.B., S.A., D.G.S.), NSF DEB-1716698 (R.K.P., D.J.B.), NSF IOS-1054675 (D.M.H.), NSF IOS-1257773 and NSF IOS-1656618 (L.B.M.); the Finnish Cultural Foundation (K.M.F.); the United States Agency for International Development (USAID) Emerging Pandemic Threats PREDICT program (J.H.E.); the Defense Advanced Research Projects Agency (DARPA D16AP00113; D.J.B., R.K.P.); the US National Institutes of General Medical Sciences IDeA Program (P20GM103474 and P30GM110732; R.K.P.); Montana University System Research Initiative (51040-MUSRI2015-03; R.K.P.); the Strategic Environmental Research and Development Program (RC-2633; R.K.P.); the James Smithson Fellowship at the Smithsonian Institution (D.A.S.); and a Sir Henry Dale Fellowship (D.G.S.), jointly funded by the Wellcome Trust and Royal Society (102507/Z/13/Z). The views, opinions and/or findings expressed are those of the authors and should not be interpreted as representing the official views or policies of the funding agencies (including the Department of Defense) or the US Government.

Footnotes

  • One contribution of 14 to a theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.

  • Accepted January 12, 2018.
  • © 2018 The Author(s)
http://royalsocietypublishing.org/licence

Published by the Royal Society. All rights reserved.

References

  1. ↵
    1. Orams MB
    . 2002 Feeding wildlife as a tourism attraction: a review of issues and impacts. Tour. Manag. 23, 281–293. (doi:10.1016/S0261-5177(01)00080-2)
    OpenUrl
  2. ↵
    1. Robb GN,
    2. McDonald RA,
    3. Chamberlain DE,
    4. Bearhop S
    . 2008 Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front. Ecol. Environ. 6, 476–484. (doi:10.1890/060152)
    OpenUrlCrossRefWeb of Science
  3. ↵
    1. Hill CM
    . 2000 Conflict of interest between people and baboons: crop raiding in Uganda. Int. J. Primatol. 21, 299–315. (doi:10.1023/A:1005481605637)
    OpenUrl
  4. ↵
    1. Elliott KH,
    2. Duffe J,
    3. Lee SL,
    4. Mineau P,
    5. Elliott JE
    . 2006 Foraging ecology of Bald Eagles at an urban landfill. Wilson J. Ornithol. 118, 380–390. (doi:10.1676/04-126.1)
    OpenUrl
  5. ↵
    1. Sutherland WJ
    . 1996 Predicting the consequences of habitat loss for migratory populations. Proc. R. Soc. Lond. B 263, 1325–1327. (doi:10.1098/rspb.1996.0194)
    OpenUrlAbstract/FREE Full Text
  6. ↵
    1. Altizer S,
    2. Bartel R,
    3. Han BA
    . 2011 Animal migration and infectious disease risk. Science 331, 296–302. (doi:10.1126/science.1194694)
    OpenUrlAbstract/FREE Full Text
    1. Oro D,
    2. Genovart M,
    3. Tavecchia G,
    4. Fowler MS,
    5. Martínez-Abraín A
    . 2013 Ecological and evolutionary implications of food subsidies from humans. Ecol. Lett. 16, 1501–1514. (doi:10.1111/ele.12187)
    OpenUrlCrossRefPubMed
  7. ↵
    1. Sutherland WJ et al.
    2016 A 2017 horizon scan of emerging issues for global conservation and biological diversity. Trends Ecol. Evol. 32, 31–40. (doi:10.1016/j.tree.2016.11.005)
    OpenUrl
  8. ↵
    1. Dallas T,
    2. Drake JM
    . 2014 Nitrate enrichment alters a Daphnia–microparasite interaction through multiple pathways. Ecol. Evol. 4, 243–250. (doi:10.1002/ece3.925)
    OpenUrl
  9. ↵
    1. Gervasi SS,
    2. Civitello DJ,
    3. Kilvitis HJ,
    4. Martin LB
    . 2015 The context of host competence: a role for plasticity in host–parasite dynamics. Trends Parasitol. 31, 419–425. (doi:10.1016/j.pt.2015.05.002)
    OpenUrlCrossRefPubMed
  10. ↵
    1. Lochmiller RL,
    2. Deerenberg C
    . 2000 Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98. (doi:10.1034/j.1600-0706.2000.880110.x)
    OpenUrlCrossRefWeb of Science
  11. ↵
    1. Brace AJ et al.
    2017 Costs of immune responses are related to host body size and lifespan. J. Exp. Zool. Part Ecol. Integr. Physiol. 2017, 1–8. (doi:10.1002/jez.2084)
    OpenUrl
  12. ↵
    1. Forbes KM,
    2. Mappes T,
    3. Sironen T,
    4. Strandin T,
    5. Stuart P,
    6. Meri S,
    7. Vapalahti O,
    8. Henttonen H,
    9. Huitu O
    . 2016 Food limitation constrains host immune responses to nematode infections. Biol. Lett. 12, 20160471. (doi:10.1098/rsbl.2016.0471)
    OpenUrlAbstract/FREE Full Text
  13. ↵
    1. Becker DJ,
    2. Hall RJ
    . 2014 Too much of a good thing: resource provisioning alters infectious disease dynamics in wildlife. Biol. Lett. 10, 20140309. (doi:10.1098/rsbl.2014.0309)
    OpenUrlAbstract/FREE Full Text
  14. ↵
    1. Forbes KM,
    2. Henttonen H,
    3. Hirvelä-Koski V,
    4. Kipar A,
    5. Mappes T,
    6. Stuart P,
    7. Huitu O
    . 2015 Food provisioning alters infection dynamics in populations of a wild rodent. Proc R Soc B 282, 20151939. (doi:10.1098/rspb.2015.1939)
    OpenUrlAbstract/FREE Full Text
  15. ↵
    1. Becker DJ,
    2. Streicker DG,
    3. Altizer S
    . 2015 Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis. Ecol. Lett. 18, 483–495. (doi:10.1111/ele.12428)
    OpenUrlCrossRefPubMed
  16. ↵
    1. Hite JL,
    2. Cressler CE
    . 2018 Resource-driven changes to host population stability alter the evolution of virulence and transmission. Phil. Trans. R. Soc. B 373, 20170087. (doi:10.1098/rstb.2017.0087)
    OpenUrlAbstract/FREE Full Text
  17. ↵
    1. Strandin T,
    2. Babayan SA,
    3. Forbes KM
    . 2018 Reviewing the effects of food provisioning on wildlife immunity. Phil. Trans. R. Soc. B 373, 20170088. (doi:10.1098/rstb.2017.0088)
    OpenUrlAbstract/FREE Full Text
  18. ↵
    1. Klasing KC
    . 2007 Nutrition and the immune system. Br. Poult. Sci. 48, 525–537. (doi:10.1080/00071660701671336)
    OpenUrlCrossRefPubMedWeb of Science
  19. ↵
    1. Cunningham-Rundles S,
    2. McNeeley DF,
    3. Moon A
    . 2005 Mechanisms of nutrient modulation of the immune response. J. Allergy Clin. Immunol. 115, 1119–1128. (doi:10.1016/j.jaci.2005.04.036)
    OpenUrlCrossRefPubMedWeb of Science
  20. ↵
    1. Becker DJ et al.
    2018 Livestock abundance predicts vampire bat demography, immune profiles and bacterial infection risk. Phil. Trans. R. Soc. B 373, 20170089. (doi:10.1098/rstb.2017.0089)
    OpenUrlAbstract/FREE Full Text
  21. ↵
    1. Cotterill GG,
    2. Cross PC,
    3. Cole EK,
    4. Fuda RK,
    5. Rogerson JD,
    6. Scurlock BM,
    7. du Toit JT
    . 2018 Winter feeding of elk in the Greater Yellowstone Ecosystem and its effects on disease dynamics. Phil. Trans. R. Soc. B 373, 20170093. (doi:10.1098/rstb.2017.0093)
    OpenUrlAbstract/FREE Full Text
  22. ↵
    1. Plowright RK,
    2. Peel AJ,
    3. Streicker DG,
    4. Gilbert AT,
    5. McCallum H,
    6. Wood J,
    7. Baker ML,
    8. Restif O
    . 2016 Transmission or within-host dynamics driving pulses of zoonotic viruses in reservoir–host populations. PLoS Negl. Trop. Dis. 10, e0004796. (doi:10.1371/journal.pntd.0004796)
    OpenUrlCrossRef
  23. ↵
    1. Blanco G,
    2. Lemus JA,
    3. García-Montijano M
    . 2011 When conservation management becomes contraindicated: impact of food supplementation on health of endangered wildlife. Ecol. Appl. 21, 2469–2477. (doi:10.1890/11-0038.1)
    OpenUrl
  24. ↵
    1. Becker DJ,
    2. Chumchal MM,
    3. Bentz AB,
    4. Platt SG,
    5. Czirják GÁ,
    6. Rainwater TR,
    7. Altizer S,
    8. Streicker DG
    . 2017 Predictors and immunological correlates of sublethal mercury exposure in vampire bats. R. Soc. Open Sci. 4, 170073. (doi:10.1098/rsos.170073)
    OpenUrlAbstract/FREE Full Text
  25. ↵
    1. Field KA,
    2. Johnson JS,
    3. Lilley TM,
    4. Reeder SM,
    5. Rogers EJ,
    6. Behr MJ,
    7. Reeder DM
    . 2015 The white-nose syndrome transcriptome: activation of anti-fungal host responses in wing tissue of hibernating little brown myotis. PLoS Pathog. 11, e1005168. (doi:10.1371/journal.ppat.1005168)
    OpenUrlCrossRefPubMed
  26. ↵
    1. Martin LB,
    2. Burgan SC,
    3. Adelman JS,
    4. Gervasi SS
    . 2016 Host competence: an organismal trait to integrate immunology and epidemiology. Integr. Comp. Biol. 56, 1238–1249. (doi:10.1093/icb/icw064)
    OpenUrlCrossRefPubMed
  27. ↵
    1. Becker D,
    2. Streicker D,
    3. Altizer S
    . 2017 Using host species traits to understand the consequences of resource provisioning for host–parasite interactions. J. Anim. Ecol. 00, 1–16. (doi:10.1111/1365-2656.12765)
    OpenUrl
  28. ↵
    1. Hoverman JT,
    2. Searle CL
    . 2016 Behavioural influences on disease risk: implications for conservation and management. Anim. Behav. 120, 263–271. (doi:10.1016/j.anbehav.2016.05.013)
    OpenUrl
  29. ↵
    1. Dobson A,
    2. Foufopoulos J
    . 2001 Emerging infectious pathogens of wildlife. Phil. Trans. R. Soc. Lond. B 356, 1001–1012. (doi:10.1098/rstb.2001.0900)
    OpenUrlAbstract/FREE Full Text
  30. ↵
    1. Moyers SC,
    2. Adelman JS,
    3. Farine DR,
    4. Thomason CA,
    5. Hawley DM
    . 2018 Feeder density enhances house finch disease transmission in experimental epidemics. Phil. Trans. R. Soc. B 373, 20170090. (doi:10.1098/rstb.2017.0090)
    OpenUrlAbstract/FREE Full Text
  31. ↵
    1. Cross PC,
    2. Cole EK,
    3. Dobson AP,
    4. Edwards WH,
    5. Hamlin KL,
    6. Luikart G,
    7. Middleton AD,
    8. Scurlock BM,
    9. White PJ
    . 2010 Probable causes of increasing brucellosis in free-ranging elk of the Greater Yellowstone Ecosystem. Ecol. Appl. 20, 278–288. (doi:10.1890/08-2062.1)
    OpenUrlCrossRefPubMed
  32. ↵
    1. Murray MH,
    2. Kidd AD,
    3. Curry SE,
    4. Hepinstall-Cymerman J,
    5. Yabsley MJ,
    6. Adams HC,
    7. Ellison T,
    8. Welch CN,
    9. Hernandez SM
    . 2018 From wetland specialist to hand-fed generalist: shifts in diet and condition with provisioning for a recently urbanized wading bird. Phil. Trans. R. Soc. B 373, 20170100. (doi:10.1098/rstb.2017.0100)
    OpenUrlAbstract/FREE Full Text
  33. ↵
    1. Epstein JH,
    2. McKee J,
    3. Shaw P,
    4. Hicks V,
    5. Micalizzi G,
    6. Daszak P,
    7. Kilpatrick AM,
    8. Kaufman G
    . 2006 The Australian white ibis (Threskiornis molucca) as a reservoir of zoonotic and livestock pathogens. EcoHealth 3, 290–298. (doi:10.1007/s10393-006-0064-2)
    OpenUrl
  34. ↵
    1. Shaw P
    . 2000 Ibis management program annual report to the ibis management. Coordination Group (IMCG), Gold Coast, Queensland. Appl. Env. Microbiol. 68, 5595–5599.
    OpenUrl
  35. ↵
    1. Satterfield DA,
    2. Marra PP,
    3. Sillett TS,
    4. Altizer S
    . 2018 Responses of migratory species and their pathogens to supplemental feeding. Phil. Trans. R. Soc. B 373, 20170094. (doi:10.1098/rstb.2017.0094)
    OpenUrlAbstract/FREE Full Text
  36. ↵
    1. Satterfield DA,
    2. Maerz JC,
    3. Altizer S
    . 2015 Loss of migratory behaviour increases infection risk for a butterfly host. Proc. R. Soc. B 282, 20141734. (doi:10.1098/rspb.2014.1734)
    OpenUrlAbstract/FREE Full Text
  37. ↵
    1. Plowright RK,
    2. Foley P,
    3. Field HE,
    4. Dobson AP,
    5. Foley JE,
    6. Eby P,
    7. Daszak P
    . 2011 Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc. R. Soc. B 278, 3703–3712. (doi:10.1098/rspb.2011.0522)
    OpenUrlAbstract/FREE Full Text
    1. Bjørn PA,
    2. Finstad B,
    3. Kristoffersen R
    . 2001 Salmon lice infection of wild sea trout and Arctic char in marine and freshwaters: the effects of salmon farms. Aquac. Res. 32, 947–962. (doi:10.1046/j.1365-2109.2001.00627.x)
    OpenUrl
  38. ↵
    1. Satterfield DA,
    2. Villablanca FX,
    3. Maerz JC,
    4. Altizer S
    . 2016 Migratory monarchs wintering in California experience low infection risk compared to monarchs breeding year-round on non-native milkweed. Integr. Comp. Biol. 56, 343–352. (doi:10.1093/icb/icw030)
    OpenUrlCrossRefPubMed
  39. ↵
    1. Epstein JH et al.
    2009 Pteropus vampyrus, a hunted migratory species with a multinational home-range and a need for regional management. J. Appl. Ecol. 46, 991–1002. (doi:10.1111/j.1365-2664.2009.01699.x)
    OpenUrlCrossRefWeb of Science
  40. ↵
    1. Gurley ES et al.
    2017 Convergence of Humans, Bats, Trees, and Culture in Nipah Virus Transmission, Bangladesh. Emerg. Infect. Dis. 23, 1446–1453. (doi:10.3201/eid2309.161922)
    OpenUrl
  41. ↵
    1. Luby SP et al.
    2006 Foodborne transmission of Nipah Virus, Bangladesh. Emerg. Infect. Dis. 12, 1888–1894. (doi:10.3201/eid1212.060732)
    OpenUrlCrossRefPubMedWeb of Science
  42. ↵
    1. Gilbert M,
    2. Xiao X,
    3. Domenech J,
    4. Lubroth J,
    5. Martin V,
    6. Slingenbergh J
    . 2006 Anatidae migration in the western Palearctic and spread of highly pathogenic avian influenza H5N1 virus. Emerg. Infect. Dis. 12, 1650. (doi:10.3201/eid1211.060223)
    OpenUrlCrossRefPubMedWeb of Science
  43. ↵
    1. Waldenström J,
    2. Bensch S,
    3. Kiboi S,
    4. Hasselquist D,
    5. Ottosson U
    . 2002 Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol. Ecol. 11, 1545–1554. (doi:10.1046/j.1365-294X.2002.01523.x)
    OpenUrlCrossRefPubMedWeb of Science
  44. ↵
    1. Brown LM,
    2. Hall RJ
    . 2018 Consequences of resource supplementation for disease risk in a partially migratory population. Phil. Trans. R. Soc. B 373, 20170095. (doi:10.1098/rstb.2017.0095)
    OpenUrlAbstract/FREE Full Text
  45. ↵
    1. Plowright RK et al.
    2015 Ecological dynamics of emerging bat virus spillover. Proc. R. Soc. B 282, 20142124. (doi:10.1098/rspb.2014.2124)
    OpenUrlAbstract/FREE Full Text
  46. ↵
    1. Páez DJ,
    2. Restif O,
    3. Eby P,
    4. Plowright RK
    . 2018 Optimal foraging in seasonal environments: implications for residency of Australian flying foxes in food-subsidized urban landscapes. Phil. Trans. R. Soc. B 373, 20170097. (doi:10.1098/rstb.2017.0097)
    OpenUrlAbstract/FREE Full Text
  47. ↵
    1. Páez DJ,
    2. Giles J,
    3. Mccallum H,
    4. Field H,
    5. Jordan D,
    6. Peel AJ,
    7. Plowright RK
    . 2017 Conditions affecting the timing and magnitude of Hendra virus shedding across pteropodid bat populations in Australia. Epidemiol. Amp. Infect. 57, 1–11. (doi:10.1017/S0950268817002138)
    OpenUrl
  48. ↵
    1. Plowright RK,
    2. Parrish CR,
    3. McCallum H,
    4. Hudson PJ,
    5. Ko AI,
    6. Graham AL,
    7. Lloyd-Smith JO
    . 2017 Pathways to zoonotic spillover. Nat. Rev. Microbiol. 15, 502–510. (doi:10.1038/nrmicro.2017.45)
    OpenUrl
  49. ↵
    1. McKinney ML
    . 2006 Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260. (doi:10.1016/j.biocon.2005.09.005)
    OpenUrlCrossRef
    1. Bradley CA,
    2. Altizer S
    . 2007 Urbanization and the ecology of wildlife diseases. Trends Ecol. Evol. 22, 95–102. (doi:10.1016/j.tree.2006.11.001)
    OpenUrlCrossRefPubMedWeb of Science
  50. ↵
    1. Sih A,
    2. Ferrari MCO,
    3. Harris DJ
    . 2011 Evolution and behavioural responses to human-induced rapid environmental change. Evol. Appl. 4, 367–387. (doi:10.1111/j.1752-4571.2010.00166.x)
    OpenUrlCrossRefPubMed
  51. ↵
    1. Armien B et al.
    2013 Hantavirus fever without pulmonary syndrome in Panama. Am. J. Trop. Med. Hyg. 89, 489–494. (doi:10.4269/ajtmh.12-0334)
    OpenUrlAbstract/FREE Full Text
  52. ↵
    1. Limongi JE et al.
    2016 Hantavirus pulmonary syndrome and rodent reservoirs in the savanna-like biome of Brazil's southeastern region. Epidemiol. Infect. 144, 1107–1116. (doi:10.1017/S095026881500237X)
    OpenUrl
  53. ↵
    1. Lee DN,
    2. Papeş M,
    3. Van Den Bussche RA
    . 2012 Present and potential future distribution of common vampire bats in the Americas and the associated risk to cattle. PLoS ONE 7, e0042466. (doi:10.1371/journal.pone.0042466)
    OpenUrl
  54. ↵
    1. Pulliam JRC et al.
    2012 Agricultural intensification, priming for persistence and the emergence of Nipah virus: a lethal bat-borne zoonosis. J. R. Soc. Interface 9, 89–101. (doi:10.1098/rsif.2011.0223)
    OpenUrlAbstract/FREE Full Text
  55. ↵
    1. Openshaw JJ,
    2. Hegde S,
    3. Sazzad HM,
    4. Khan SU,
    5. Hossain MJ,
    6. Epstein JH,
    7. Daszak P,
    8. Gurley ES,
    9. Luby SP
    . 2015 Increased morbidity and mortality in domestic animals eating dropped and bitten fruit in Bangladeshi villages: implications for zoonotic disease transmission. EcoHealth 13, 39–48. (doi:10.1007/s10393-015-1080-x)
    OpenUrl
  56. ↵
    1. Chowdhury S et al.
    2014 Serological evidence of Henipavirus exposure in cattle, goats and pigs in Bangladesh. PLoS Negl. Trop. Dis. 8, e3302. (doi:10.1371/journal.pntd.0003302)
    OpenUrl
  57. ↵
    1. Weissinger MD,
    2. Theimer TC,
    3. Bergman DL,
    4. Deliberto TJ
    . 2009 Nightly and seasonal movements, seasonal home range, and focal location photo-monitoring of urban striped skunks (Mephitis mephitis): implications for rabies transmission. J. Wildl. Dis. 45, 388–397. (doi:10.7589/0090-3558-45.2.388)
    OpenUrlAbstract/FREE Full Text
  58. ↵
    1. Totton SC,
    2. Tinline RR,
    3. Rosatte RC,
    4. Bigler LL
    . 2002 Contact rates of raccoons (Procyon lotor) at a communal feeding site in rural eastern Ontario. J. Wildl. Dis. 38, 313–319. (doi:10.7589/0090-3558-38.2.313)
    OpenUrlAbstract
  59. ↵
    1. Maxwell MJ,
    2. de Carvalho MHF,
    3. Hoet AE,
    4. Vigilato MA,
    5. Pompei JC,
    6. Cosivi O,
    7. Victor J
    . 2017 Building the road to a regional zoonoses strategy: a survey of zoonoses programmes in the Americas. PLoS ONE 12, e0174175.
    OpenUrl
  60. ↵
    1. Benavides JA,
    2. Valderrama W,
    3. Streicker DG
    . 2016 Spatial expansions and travelling waves of rabies in vampire bats. Proc R Soc B 283, 20160328. (doi:10.1098/rspb.2016.0328)
    OpenUrlAbstract/FREE Full Text
  61. ↵
    1. Middleton D et al.
    2014 Hendra virus vaccine, a one health approach to protecting horse, human, and environmental health. Emerg. Infect. Dis. 20, 372. (doi:10.3201/eid2003.131159)
    OpenUrlCrossRefPubMed
  62. ↵
    1. Jones-Engel L et al.
    2006 Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerg. Infect. Dis. 12, 900–906. (doi:10.3201/eid1206.060030)
    OpenUrlCrossRefPubMed
  63. ↵
    1. Mafuyai HB,
    2. Barshep Y,
    3. Audu BS,
    4. Kumbak D,
    5. Ojobe TO
    . 2013 Baboons as potential reservoirs of zoonotic gastrointestinal parasite infections at Yankari National Park, Nigeria. Afr. Health Sci. 13, 252–254.
    OpenUrl
  64. ↵
    1. Ryan SJ,
    2. Brashares JS,
    3. Walsh C,
    4. Milbers K,
    5. Kilroy C,
    6. Chapman CA
    . 2012 A Survey of gastrointestinal parasites of olive baboons (Papio anubis) in human settlement areas of Mole National Park, Ghana. J. Parasitol. 98, 885–888. (doi:10.1645/GE-2976.1)
    OpenUrlPubMed
  65. ↵
    1. Hall RJ,
    2. Brown LM,
    3. Altizer S
    . 2016 Modeling vector-borne disease risk in migratory animals under climate change. Integr. Comp. Biol. 56, 353–364. (doi:10.1093/icb/icw049)
    OpenUrlCrossRefPubMed
    1. Lafferty KD,
    2. Mordecai EA
    . 2016 The rise and fall of infectious disease in a warmer world. F1000Research 5, F1000. (doi:10.12688/f1000research.8766.1)
    OpenUrlCrossRef
    1. Kilpatrick AM,
    2. Briggs CJ,
    3. Daszak P
    . 2010 The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol. Evol. 25, 109–118. (doi:10.1016/j.tree.2009.07.011)
    OpenUrlCrossRefPubMedWeb of Science
  66. ↵
    1. Frick WF,
    2. Pollock JF,
    3. Hicks AC,
    4. Langwig KE,
    5. Reynolds DS,
    6. Turner GG,
    7. Butchkoski CM,
    8. Kunz TH
    . 2010 An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682. (doi:10.1126/science.1188594)
    OpenUrlAbstract/FREE Full Text
  67. ↵
    1. Civitello DJ,
    2. Allman BE,
    3. Morozumi C,
    4. Rohr JR
    . 2018 Assessing the direct and indirect effects of food provisioning and nutrient enrichment on wildlife infectious disease dynamics. Phil. Trans. R. Soc. B 373, 20170101. (doi:10.1098/rstb.2017.0101)
    OpenUrlAbstract/FREE Full Text
  68. ↵
    1. Hall SR,
    2. Knight CJ,
    3. Becker CR,
    4. Duffy MA,
    5. Tessier AJ,
    6. Caceres CE
    . 2009 Quality matters: resource quality for hosts and the timing of epidemics. Ecol. Lett. 12, 118–128. (doi:10.1111/j.1461-0248.2008.01264.x)
    OpenUrlCrossRefPubMedWeb of Science
  69. ↵
    1. Becker DJ,
    2. Hall RJ
    . 2016 Heterogeneity in patch quality buffers metapopulations from pathogen impacts. Theor. Ecol. 9, 197–205. (doi:10.1007/s12080-015-0284-6)
    OpenUrl
  70. ↵
    1. Leach CB,
    2. Webb CT,
    3. Cross PC
    . 2016 When environmentally persistent pathogens transform good habitat into ecological traps. R. Soc. Open Sci. 3, 160051. (doi:10.1098/rsos.160051)
    OpenUrlAbstract/FREE Full Text
  71. ↵
    1. McCALLUM H
    . 2016 Models for managing wildlife disease. Parasitology 143, 805–820. (doi:10.1017/S0031182015000980)
    OpenUrl
  72. ↵
    1. Wright AN,
    2. Gompper ME
    . 2005 Altered parasite assemblages in raccoons in response to manipulated resource availability. Oecologia 144, 148–156. (doi:10.1007/s00442-005-0018-3)
    OpenUrlCrossRefPubMedWeb of Science
  73. ↵
    1. Wilcoxen TE et al.
    2015 Effects of bird-feeding activities on the health of wild birds. Conserv. Physiol. 3, cov058. (doi:10.1093/conphys/cov058)
    OpenUrl
  74. ↵
    1. Galbraith JA,
    2. Stanley MC,
    3. Jones DN,
    4. Beggs JR
    . 2017 Experimental feeding regime influences urban bird disease dynamics. J. Avian Biol. 48, 700–713. (doi:10.1111/jav.01076)
    OpenUrl
  75. ↵
    1. Martin LB,
    2. Navara KJ,
    3. Weil ZM,
    4. Nelson RJ
    . 2007 Immunological memory is compromised by food restriction in deer mice Peromyscus maniculatus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R316–R320. (doi:10.1152/ajpregu.00386.2006)
    OpenUrlCrossRef
  76. ↵
    1. G Diego,
    2. B Henrik
    1. Martin LB,
    2. Boruta M
    . 2013 The impacts of urbanization on avian disease transmission and emergence. In Avian Urban Ecol. Behav. Physiol. Adapt (eds G Diego, B Henrik), pp. 116–128. Oxford, UK: Oxford University Press.
  77. ↵
    1. Delpietro HA,
    2. Marchevsky N,
    3. Simonetti E
    . 1992 Relative population densities and predation of the common vampire bat (Desmodus rotundus) in natural and cattle-raising areas in north-east Argentina. Prev. Vet. Med. 14, 13–20. (doi:10.1016/0167-5877(92)90080-Y)
    OpenUrlCrossRef
  78. ↵
    1. Streicker DG,
    2. Allgeier JE
    . 2016 Foraging choices of vampire bats in diverse landscapes: potential implications for land-use change and disease transmission. J. Appl. Ecol. 53, 1280–1288. (doi:10.1111/1365-2664.12690)
    OpenUrl
  79. ↵
    1. Crespo RF,
    2. Linhart SB,
    3. Burns RJ,
    4. Mitchell GC
    . 1972 Foraging behavior of the common vampire bat related to moonlight. J. Mammal. 53, 366. (doi:10.2307/1379175)
    OpenUrlCrossRefWeb of Science
  80. ↵
    1. Pedersen AB,
    2. Greives TJ
    . 2008 The interaction of parasites and resources cause crashes in a wild mouse population. J. Anim. Ecol. 77, 370–377. (doi:10.1111/j.1365-2656.2007.01321.x)
    OpenUrlCrossRefPubMedWeb of Science
    1. Forbes KM,
    2. Stuart P,
    3. Mappes T,
    4. Henttonen H,
    5. Huitu O
    . 2014 Food resources and intestinal parasites as limiting factors for boreal vole populations during winter. Ecology 95, 3139–3148. (doi:10.1890/13-2381.1)
    OpenUrlCrossRef
    1. Blount JD,
    2. Metcalfe NB,
    3. Birkhead TR,
    4. Surai PF
    . 2003 Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300, 125–127. (doi:10.1126/science.1082142)
    OpenUrlAbstract/FREE Full Text
  81. ↵
    1. Blount JD,
    2. Surai PF,
    3. Nager RG,
    4. Houston DC,
    5. Møller AP,
    6. Trewby ML,
    7. Kennedy MW
    . 2002 Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc. R. Soc. B 269, 29–36. (doi:10.1098/rspb.2001.1840)
    OpenUrlAbstract/FREE Full Text
  82. ↵
    1. Lipsitch M,
    2. Siller S,
    3. Nowak MA
    . 1996 The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 1729–1741. (doi:10.1111/j.1558-5646.1996.tb03560.x)
    OpenUrlCrossRefWeb of Science
  83. ↵
    1. Vale PF,
    2. Choisy M,
    3. Little TJ
    . 2013 Host nutrition alters the variance in parasite transmission potential. Biol. Lett. 9, 20121145. (doi:10.1098/rsbl.2012.1145)
    OpenUrlAbstract/FREE Full Text
  84. ↵
    1. Brown MJF,
    2. Loosli R,
    3. Schmid-Hempel P
    . 2000 Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427. (doi:10.1034/j.1600-0706.2000.910302.x)
    OpenUrlCrossRefWeb of Science
  85. ↵
    1. Miller MR,
    2. White A,
    3. Boots M
    . 2006 The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism. Evolution 60, 945–956. (doi:10.1111/j.0014-3820.2006.tb01173.x)
    OpenUrlCrossRefPubMedWeb of Science
  86. ↵
    1. Kau AL,
    2. Ahern PP,
    3. Griffin NW,
    4. Goodman AL,
    5. Gordon JI
    . 2011 Human nutrition, the gut microbiome, and immune system: envisioning the future. Nature 474, 327. (doi:10.1038/nature10213)
    OpenUrlCrossRefPubMedWeb of Science
  87. ↵
    1. Knutie SA,
    2. Wilkinson CL,
    3. Kohl KD,
    4. Rohr JR
    . 2017 Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nat. Commun. 8, 86. (doi:10.1038/s41467-017-00119-0)
    OpenUrlCrossRef
  88. ↵
    1. Henderson G,
    2. Cox F,
    3. Ganesh S,
    4. Jonker A,
    5. Young W,
    6. Janssen PH
    . 2015 Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci. Rep. 5, 14567. (doi:10.1038/srep14567)
    OpenUrlCrossRefPubMed
  89. ↵
    1. Gomez A et al.
    2015 Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol. Ecol. 24, 2551–2565. (doi:10.1111/mec.13181)
    OpenUrlCrossRef
  90. ↵
    1. Angelakis E et al.
    2016 Gut microbiome and dietary patterns in different Saudi populations and monkeys. Sci. Rep. 6, srep32191. (doi:10.1038/srep32191)
    OpenUrl
  91. ↵
    1. Wobeser G,
    2. Rainnie DJ
    . 1987 Epizootic necrotic enteritis in wild geese. J. Wildl. Dis. 23, 376–385. (doi:10.7589/0090-3558-23.3.376)
    OpenUrlAbstract
  92. ↵
    1. Breton J,
    2. Massart S,
    3. Vandamme P,
    4. De Brandt E,
    5. Pot B,
    6. Foligné B
    . 2013 Ecotoxicology inside the gut: impact of heavy metals on the mouse microbiome. BMC Pharmacol. Toxicol. 14, 62. (doi:10.1186/2050-6511-14-62)
    OpenUrlCrossRefPubMed
  93. ↵
    1. Cox DTC,
    2. Gaston KJ
    . 2018 Human–nature interactions and the consequences and drivers of provisioning wildlife. Phil. Trans. R. Soc. B 373, 20170092. (doi:10.1098/rstb.2017.0092)
    OpenUrlAbstract/FREE Full Text
  94. ↵
    1. Jones D
    . 2011 An appetite for connection: why we need to understand the effect and value of feeding wild birds. Emu 111, i–vii. (doi:10.1071/MUv111n2_ED)
    OpenUrl
  95. ↵
    1. Fuentes A
    . 2011 Monkeys on the edge: ecology and management of long-tailed macaques and their interface with humans. Cambridge, UK: Cambridge University Press.
  96. ↵
    1. Lepczyk CA,
    2. Warren PS,
    3. Machabée L,
    4. Kinzig AP,
    5. Mertig AG
    . 2012 Who feeds the birds: a comparison across regions. Stud. Avian Biol. 45, 267–284.
    OpenUrl
  97. ↵
    1. Reynolds SJ,
    2. Galbraith JA,
    3. Smith JA,
    4. Jones DN
    . 2017 Garden bird feeding: insights and prospects from a north-south comparison of this global urban phenomenon. Front. Ecol. Evol. 5, 24. (doi:10.3389/fevo.2017.00024)
    OpenUrl
  98. ↵
    1. Curtin S
    . 2009 Wildlife tourism: the intangible, psychological benefits of human–wildlife encounters. Curr. Issues Tour. 12, 451–474. (doi:10.1080/13683500903042857)
    OpenUrl
  99. ↵
    1. Dubois S,
    2. Fraser D
    . 2013 A framework to evaluate wildlife feeding in research, wildlife management, tourism and recreation. Animals 3, 978–994. (doi:10.3390/ani3040978)
    OpenUrl
  100. ↵
    1. Galbraith JA,
    2. Beggs JR,
    3. Jones DN,
    4. McNaughton EJ,
    5. Krull CR,
    6. Stanley MC
    . 2014 Risks and drivers of wild bird feeding in urban areas of New Zealand. Biol. Conserv. 180, 64–74. (doi:10.1016/j.biocon.2014.09.038)
    OpenUrl
  101. ↵
    1. Goddard MA,
    2. Dougill AJ,
    3. Benton TG
    . 2013 Why garden for wildlife? Social and ecological drivers, motivations and barriers for biodiversity management in residential landscapes. Ecol. Econ. 86, 258–273. (doi:10.1016/j.ecolecon.2012.07.016)
    OpenUrl
  102. ↵
    1. Cox DT,
    2. Gaston KJ
    . 2016 Urban bird feeding: connecting people with nature. PLoS ONE 11, e0158717.
    OpenUrl
  103. ↵
    1. Muehlenbein MP
    . 2017 Primates on display: potential disease consequences beyond bushmeat. Am. J. Phys. Anthropol. 162, 32–43. (doi:10.1002/ajpa.23145)
    OpenUrl
  104. ↵
    1. Lawson B,
    2. Robinson RA,
    3. Toms MP,
    4. Risely K,
    5. MacDonald S,
    6. Cunningham AA
    . 2018 Health hazards to wild birds and risk factors associated with anthropogenic food provisioning. Phil. Trans. R. Soc. B 373, 20170091. (doi:10.1098/rstb.2017.0091)
    OpenUrlAbstract/FREE Full Text
  105. ↵
    1. Cox DT,
    2. Shanahan DF,
    3. Hudson HL,
    4. Plummer KE,
    5. Siriwardena GM,
    6. Fuller RA,
    7. Anderson K,
    8. Hancock S,
    9. Gaston KJ
    . 2017 Doses of neighborhood nature: the benefits for mental health of living with nature. BioScience 67, 147–155.
    OpenUrlCrossRef
  106. ↵
    1. Newton I
    . 2010 The migration ecology of birds. New York, NY: Academic press.
  107. ↵
    1. Robb GN,
    2. McDonald RA,
    3. Chamberlain DE,
    4. Reynolds SJ,
    5. Harrison TJE,
    6. Bearhop S
    . 2008 Winter feeding of birds increases productivity in the subsequent breeding season. Biol. Lett. 4, 220–223. (doi:10.1098/rsbl.2007.0622)
    OpenUrlAbstract/FREE Full Text
  108. ↵
    1. Galbraith JA,
    2. Beggs JR,
    3. Jones DN,
    4. Stanley MC
    . 2015 Supplementary feeding restructures urban bird communities. Proc. Natl Acad. Sci. USA 112, E2648–E2657. (doi:10.1073/pnas.1501489112)
    OpenUrlAbstract/FREE Full Text
  109. ↵
    1. Greig EI,
    2. Wood EM,
    3. Bonter DN
    . 2017 Winter range expansion of a hummingbird is associated with urbanization and supplementary feeding. Proc R Soc B 284, 20170256. (doi:10.1098/rspb.2017.0256)
    OpenUrlAbstract/FREE Full Text
  110. ↵
    1. Fuller RA,
    2. Warren PH,
    3. Armsworth PR,
    4. Barbosa O,
    5. Gaston KJ
    . 2008 Garden bird feeding predicts the structure of urban avian assemblages. Divers. Distrib. 14, 131–137. (doi:10.1111/j.1472-4642.2007.00439.x)
    OpenUrlCrossRefWeb of Science
  111. ↵
    1. Smith JS
    . 1996 New aspects of rabies with emphasis on epidemiology, diagnosis, and prevention of the disease in the United States. Clin. Microbiol. Rev. 9, 166.
    OpenUrlFREE Full Text
  112. ↵
    1. Jones-Engel L et al.
    2008 Diverse contexts of zoonotic transmission of simian foamy viruses in Asia. Emerg. Infect. Dis. 14, 1200–1208. (doi:10.3201/eid1408.071430)
    OpenUrlCrossRefPubMed
  113. ↵
    1. Köndgen S et al.
    2008 Pandemic human viruses cause decline of endangered great apes. Curr. Biol. 18, 260–264. (doi:10.1016/j.cub.2008.01.012)
    OpenUrlCrossRefPubMedWeb of Science
  114. ↵
    1. Lee M-H et al.
    2015 Macacine Herpesvirus 1 in long-tailed macaques, Malaysia, 2009–2011. Emerg. Infect. Dis. 21, 1107. (doi:10.3201/eid2107.140162)
    OpenUrl
  115. ↵
    1. Schweiger A et al.
    2007 Human alveolar echinococcosis after fox population increase, Switzerland. Emerg. Infect. Dis. 13, 878. (doi:10.3201/eid1306.061074)
    OpenUrlCrossRefPubMedWeb of Science
  116. ↵
    1. Luby SP et al.
    2009 Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001–2007. Emerg. Infect. Dis. 15, 1229. (doi:10.3201/eid1508.081237)
    OpenUrlCrossRefPubMedWeb of Science
  117. ↵
    1. Chua KB,
    2. Chua BH,
    3. Wang CW
    . 2002 Anthropogenic deforestation, El Niiio and the emergence of Nipah virus in Malaysia. Malays. J. Pathol. 24, 15–21.
    OpenUrlPubMed
  118. ↵
    1. Messenger AM,
    2. Barnes AN,
    3. Gray GC
    . 2014 Reverse zoonotic disease transmission (zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLoS ONE 9, e89055. (doi:10.1371/journal.pone.0089055)
    OpenUrlCrossRefPubMed
  119. ↵
    1. Epstein JH,
    2. Price JT
    . 2009 The significant but understudied impact of pathogen transmission from humans to animals. Mt. Sinai J. Med. J. Transl. Pers. Med. 76, 448–455. (doi:10.1002/msj.20140)
    OpenUrl
  120. ↵
    1. Ghai RR,
    2. Simons ND,
    3. Chapman CA,
    4. Omeja PA,
    5. Davies TJ,
    6. Ting N,
    7. Goldberg TL
    . 2014 Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Negl. Trop. Dis. 8, e3256. (doi:10.1371/journal.pntd.0003256)
    OpenUrlCrossRefPubMed
  121. ↵
    1. Kao RR,
    2. Haydon DT,
    3. Lycett SJ,
    4. Murcia PR
    . 2014 Supersize me: how whole-genome sequencing and big data are transforming epidemiology. Trends Microbiol. 22, 282–291. (doi:10.1016/j.tim.2014.02.011)
    OpenUrlCrossRefPubMed
  122. ↵
    1. Faria NR,
    2. Suchard MA,
    3. Rambaut A,
    4. Streicker DG,
    5. Lemey P
    . 2013 Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints. Phil. Trans. R. Soc. B 368, 20120196. (doi:10.1098/rstb.2012.0196)
    OpenUrlAbstract/FREE Full Text
  123. ↵
    1. Khan SU,
    2. Gurley ES,
    3. Hossain MJ,
    4. Nahar N,
    5. Sharker MAY,
    6. Luby SP
    . 2012 A randomized controlled trial of interventions to impede date palm sap contamination by bats to prevent Nipah virus transmission in Bangladesh. PLoS ONE 7, e42689. (doi:10.1371/journal.pone.0042689)
    OpenUrlCrossRefPubMed
  124. ↵
    1. Nahar N,
    2. Mondal UK,
    3. Sultana R,
    4. Hossain MJ,
    5. Khan MSU,
    6. Gurley ES,
    7. Oliveras E,
    8. Luby SP
    . 2013 Piloting the use of indigenous methods to prevent Nipah virus infection by interrupting bats' access to date palm sap in Bangladesh. Health Promot. Int. 28, 378–386. (doi:10.1093/heapro/das020)
    OpenUrlCrossRefPubMed
  125. ↵
    1. Janes CR,
    2. Corbett KK,
    3. Jones JH,
    4. Trostle J
    . 2012 Emerging infectious diseases: the role of social sciences. Lancet 380, 1884–1886. (doi:10.1016/S0140-6736(12)61725-5)
    OpenUrlPubMed
  126. ↵
    1. Creech TG,
    2. Cross PC,
    3. Scurlock BM,
    4. Maichak EJ,
    5. Rogerson JD,
    6. Henningsen JC,
    7. Creel S
    . 2012 Effects of low-density feeding on elk–fetus contact rates on Wyoming feedgrounds. J. Wildl. Manag. 76, 877–886. (doi:10.1002/jwmg.331)
    OpenUrl
  127. ↵
    1. Murray MH,
    2. Becker DJ,
    3. Hall RJ,
    4. Hernandez SM
    . 2016 Wildlife health and supplemental feeding: a review and management recommendations. Biol. Conserv. 204, 163–174. (doi:10.1016/j.biocon.2016.10.034)
    OpenUrl
  128. ↵
    1. Soulsbury CD,
    2. White PCL
    . 2016 Human–wildlife interactions in urban areas: a review of conflicts, benefits and opportunities. Wildl. Res. 42, 541–553. (doi:10.1071/WR14229)
    OpenUrl
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5 May 2018
Volume 373, issue 1745
Philosophical Transactions of the Royal Society B: Biological Sciences: 373 (1745)
  • Table of Contents
Theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’ compiled and edited by Daniel J. Becker, Richard J. Hall, Kristian M. Forbes, Raina K. Plowright and Sonia M. Altizer

Keywords

resource subsidy
anthropogenic change
human feeding of wildlife
pathogen transmission
within-host dynamics
cross-species transmission
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Food for contagion: synthesis and future directions for studying host–parasite responses to resource shifts in anthropogenic environments
Sonia Altizer, Daniel J. Becker, Jonathan H. Epstein, Kristian M. Forbes, Thomas R. Gillespie, Richard J. Hall, Dana M. Hawley, Sonia M. Hernandez, Lynn B. Martin, Raina K. Plowright, Dara A. Satterfield, Daniel G. Streicker
Phil. Trans. R. Soc. B 2018 373 20170102; DOI: 10.1098/rstb.2017.0102. Published 12 March 2018
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Review article:

Food for contagion: synthesis and future directions for studying host–parasite responses to resource shifts in anthropogenic environments

Sonia Altizer, Daniel J. Becker, Jonathan H. Epstein, Kristian M. Forbes, Thomas R. Gillespie, Richard J. Hall, Dana M. Hawley, Sonia M. Hernandez, Lynn B. Martin, Raina K. Plowright, Dara A. Satterfield, Daniel G. Streicker
Phil. Trans. R. Soc. B 2018 373 20170102; DOI: 10.1098/rstb.2017.0102. Published 12 March 2018

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