Urbanisation and agriculture cause declines for many wildlife, but some species benefit from novel resources, especially food, provided in human-dominated habitats. Resulting shifts in wildlife ecology can alter infectious disease dynamics and create opportunities for cross-species transmission, yet predicting host–pathogen responses to resource provisioning is challenging. Factors enhancing transmission, such as increased aggregation, could be offset by better host immunity due to improved nutrition. Here, we conduct a review and meta-analysis to show that food provisioning results in highly heterogeneous infection outcomes that depend on pathogen type and anthropogenic food source. We also find empirical support for behavioural and immune mechanisms through which human-provided resources alter host exposure and tolerance to pathogens. A review of recent theoretical models of resource provisioning and infection dynamics shows that changes in host contact rates and immunity produce strong non-linear responses in pathogen invasion and prevalence. By integrating results of our meta-analysis back into a theoretical framework, we find provisioning amplifies pathogen invasion under increased host aggregation and tolerance, but reduces transmission if provisioned food decreases dietary exposure to parasites. These results carry implications for wildlife disease management and highlight areas for future work, such as how resource shifts might affect virulence evolution.
Body condition metrics are widely used to infer animal health and to assess costs of parasite infection. Since parasites harm their hosts, ecologists might expect negative relationships between infection and condition in wildlife, but this assumption is challenged by studies showing positive or null condition–infection relationships. Here, we outline common condition metrics used by ecologists in studies of parasitism, and consider mechanisms that cause negative, positive, and null condition–infection relationships in wildlife systems. We then perform a meta‐analysis of 553 condition–infection relationships from 187 peer‐reviewed studies of animal hosts, analysing observational and experimental records separately, and noting whether authors measured binary infection status or intensity. Our analysis finds substantial heterogeneity in the strength and direction of condition–infection relationships, a small, negative average effect size that is stronger in experimental studies, and evidence for publication bias towards negative relationships. The strongest predictors of variation in study outcomes are host thermoregulation and the methods used to evaluate body condition. We recommend that studies aiming to assess parasite impacts on body condition should consider host–parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.
Spillover of a pathogen from a wildlife reservoir into a human or livestock host requires the pathogen to overcome a hierarchical series of barriers. Interventions aimed at one or more of these barriers may be able to prevent the occurrence of spillover. Here, we demonstrate how interventions that target the ecological context in which spillover occurs (i.e. ecological interventions) can complement conventional approaches like vaccination, treatment, disinfection and chemical control. Accelerating spillover owing to environmental change requires effective, affordable, durable and scalable solutions that fully harness the complex processes involved in cross-species pathogen spillover. This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’.
Old World fruit bats (Chiroptera: Pteropodidae) provide critical pollination and seed dispersal services to forest ecosystems across Africa, Asia, and Australia. In each of these regions, pteropodids have been identified as natural reservoir hosts for henipaviruses. The genus Henipavirus includes Hendra virus and Nipah virus, which regularly spill over from bats to domestic animals and humans in Australia and Asia, and a suite of largely uncharacterized African henipaviruses. Rapid change in fruit bat habitat and associated shifts in their ecology and behavior are well documented, with evidence suggesting that altered diet, roosting habitat, and movement behaviors are increasing spillover risk of bat-borne viruses. We review the ways that changing resource landscapes affect the processes that culminate in cross-species transmission of henipaviruses, from reservoir host density and distribution to within-host immunity and recipient host exposure. We evaluate existing evidence and highlight gaps in knowledge that are limiting our understanding of the ecological drivers of henipavirus spillover. When considering spillover in the context of land-use change, we emphasize that it is especially important to disentangle the effects of habitat loss and resource provisioning on these processes, and to jointly consider changes in resource abundance, quality, and composition.
Provisioning of abundant food resources in human-altered landscapes can have profound effects on wildlife ecology, with important implications for pathogen transmission. While empirical studies have quantified the effects of provisioning on host behaviour and immunology, the net interactive effect of these components on host-pathogen dynamics is unknown. We use simple compartmental models to investigate how provisioning-induced changes to host demography, contact behaviour and immune defence influence pathogen invasion and persistence. We show that pathogen invasion success and equilibrium prevalence depend critically on how provisioning affects host immune defence and that moderate levels of provisioning can lead to drastically different outcomes of pathogen extinction or maximizing prevalence. These results highlight the need for further empirical studies to fully understand how provisioning affects pathogen transmission in urbanized environments.
The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre‐empt infectious disease risks, especially in the context of how large‐scale factors such as urbanization affect defence by changing environmental conditions. We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large‐scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small‐scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods. We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence. We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed‐effects models that account for spatial variability while also allowing researchers to account for both individual‐ and habitat‐level covariates. We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large‐scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large‐scale field studies with small‐scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta‐analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual‐ to habitat‐level insights about the drivers of immu...
Urban development can alter resource availability, land use, and community composition, which, in turn, influences wildlife health. Generalizable relationships between wildlife health and urbanization have yet to be quantified and could vary across different measures of health and among species. We present a phylogenetic meta‐analysis of 516 comparisons of the toxicant loads, parasitism, body condition, or stress of urban and non‐urban wildlife populations reported in 106 studies spanning 81 species in 30 countries. We found a small but significant negative relationship between urbanization and wildlife health, driven by considerably higher toxicant loads and greater parasite abundance, greater parasite diversity, and/or greater likelihood of infection by parasites transmitted through close contact. Invertebrates and amphibians were particularly affected, with urban populations having higher toxicant loads and greater physiological stress than their non‐urban counterparts. We also found strong geographic and taxonomic bias in research effort, highlighting future research needs. Our results suggest that some types of health risks are more pronounced for wildlife in urban areas, which could have important implications for conservation.
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