Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis

Urbanisation and agriculture cause declines for many wildlife, but some species benefit from novelresources, especially food, provided in human-dominated habitats. Resulting shifts in wildlife ecol-ogy can alter infectious disease dynamics and create opportunities for cross-species transmission,yet predicting host–pathogen responses to resource provisioning is challenging. Factors enhancingtransmission, such as increased aggregation, could be offset by better host immunity due toimproved nutrition. Here, we conduct a review and meta-analysis to show that food provisioningresults in highly heterogeneous infection outcomes that depend on pathogen type and anthropo-genic food source. We also find empirical support for behavioural and immune mechanismsthrough which human-provided resources alter host exposure and tolerance to pathogens. Areview of recent theoretical models of resource provisioning and infection dynamics shows thatchanges in host contact rates and immunity produce strong non-linear responses in pathogen inva-sion and prevalence. By integrating results of our meta-analysis back into a theoretical frame-work, we find provisioning amplifies pathogen invasion under increased host aggregation andtolerance, but reduces transmission if provisioned food decreases dietary exposure to parasites.These results carry implications for wildlife disease management and highlight areas for futurework, such as how resource shifts might affect virulence evolution

An eco‐epidemiological modeling approach to investigate dilution effect in two different tick‐borne pathosystems

Disease (re)emergence appears to be driven by biodiversity decline and environmental change. As a result, it is increasingly important to study host-pathogen interactions within the context of their ecology and evolution. The dilution effect is the concept that higher biodiversity decreases pathogen transmission. It has been observed especially in zoonotic vector-borne pathosystems, yet evidence against it has been found. In particular, it is still debated how the community (dis)assembly assumptions and the degree of generalism of vectors and pathogens affect the direction of the biodiversity-pathogen transmission relationship. The aim of this study was to use empirical data and mechanistic models to investigate dilution mechanisms in two rodent-tick-pathogen systems differing in their vector degree of generalism. A community was assembled to include ecological interactions that expand from purely additive to purely substitutive. Such systems are excellent candidates to analyze the link between vector ecology, community (dis)assembly dynamics, and pathogen transmission. To base our mechanistic models on empirical data, rodent live-trapping, including tick sampling, was conducted in Wales across two seasons for three consecutive years. We have developed a deterministic single-vector, multi-host compartmental model that includes ecological relationships with non-host species, uniquely integrating theoretical and observational approaches. To describe pathogen transmission across a gradient of community diversity, the model was populated with parameters describing five different scenarios differing in ecological complexity; each based around one of the pathosystems: Ixodes ricinus (generalist tick) - Borrelia burgdorferi and I. trianguliceps (small mammals specialist tick) - Babesia microti. The results suggested that community composition and inter-specific dynamics affected pathogen transmission with different dilution outcomes depending on the vector degree of generalism. The model provides evidence that dilution and amplification effects are not mutually exclusive in the same community, but depend on vector ecology and the epidemiological output considered (i.e. the “risk” of interest). In our scenarios, more functionally diverse communities resulted in fewer infectious rodents, supporting the dilution effect. In the pathosystem with generalist vector we identified a hump shaped relationship between diversity and infections in hosts, while for that characterized by specialist tick, this relationship was more complex and more dependent upon specific parameter values

Spatial disease dynamics of free-living pathogens under pathogen predation

The epidemiological dynamics of potentially free-living pathogens are often studied with respect to a specific pathogen species (e.g., cholera) and most studies concentrate only on host-pathogen interactions. Here we show that metacommunity-level interactions can alter conventional spatial disease dynamics. We introduce a pathogen eating consumer species and investigate a deterministic epidemiological model of two habitat patches, where both patches can be occupied by hosts, pathogens, and consumers of free-living pathogens. An isolated habitat patch shows periodic disease outbreaks in the host population, arising from cyclic consumer-pathogen dynamics. On the other hand, consumer dispersal between the patches generate asymmetric disease prevalence, such that the host population in one patch stays disease-free, while disease outbreaks occur in the other patch. Such asymmetry can also arise with host dispersal, where infected hosts carry pathogens to the other patch. This indirect movement of pathogens causes also a counter-intuitive effect: decreasing morbidity in a focal patch under increasing pathogen immigration. Our results underline that community-level interactions influence disease dynamics and consistent spatial asymmetry can arise also in spatially homogeneous systems.Peer reviewe

Effects of an Infectious Fungus, Batrachochytrium dendrobatidis, on Amphibian Predator-Prey Interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey

Wolves contribute to disease control in a multi-host system

We combine model results with field data for a system of wolves (Canis lupus) that prey on wild boar (Sus scrofa), a wildlife reservoir of tuberculosis, to examine how predation may contribute to disease control in multi-host systems. Results show that predation can lead to a marked reduction in the prevalence of infection without leading to a reduction in host population density since mortality due to predation can be compensated by a reduction in disease induced mortality. A key finding therefore is that a population that harbours a virulent infection can be regulated at a similar density by disease at high prevalence or by predation at low prevalence. Predators may therefore provide a key ecosystem service which should be recognised when considering human-carnivore conflicts and the conservation and re-establishment of carnivore populations

Behavioral Immunity Suppresses an Epizootic in Caribbean Spiny Lobsters

Sociality has evolved in a wide range of animal taxa but infectious diseases spread rapidly in populations of aggregated individuals, potentially negating the advantages of their social interactions. To disengage from the coevolutionary struggle with pathogens, some hosts have evolved various forms of behavioral immunity ; yet, the effectiveness of such behaviors in controlling epizootics in the wild is untested. Here we show how one form of behavioral immunity (i.e., the aversion of diseased conspecifics) practiced by Caribbean spiny lobsters (Panulirus argus) when subject to the socially transmitted PaV1 virus, appears to have prevented an epizootic over a large seascape. We capitalized on a natural experiment in which a die-off of sponges in the Florida Keys (USA) resulted in a loss of shelters for juvenile lobsters over a ~2500km2 region. Lobsters were thus concentrated in the few remaining shelters, presumably increasing their exposure to the contagious virus. Despite this spatial reorganization of the population, viral prevalence in lobsters remained unchanged after the sponge die-off and for years thereafter. A field experiment in which we introduced either a healthy or PaV1-infected lobster into lobster aggregations in natural dens confirmed that spiny lobsters practice behavioral immunity. Healthy lobsters vacated dens occupied by PaV1-infected lobsters despite the scarcity of alternative shelters and the higher risk of predation they faced when searching for a new den. Simulations from a spatially-explicit, individual-based model confirmed our empirical results, demonstrating the efficacy of behavioral immunity in preventing epizootics in this system

Behavioral Immunity Suppresses an Epizootic in Caribbean Spiny Lobsters

Sociality has evolved in a wide range of animal taxa but infectious diseases spread rapidly in populations of aggregated individuals, potentially negating the advantages of their social interactions. To disengage from the coevolutionary struggle with pathogens, some hosts have evolved various forms of behavioral immunity ; yet, the effectiveness of such behaviors in controlling epizootics in the wild is untested. Here we show how one form of behavioral immunity (i.e., the aversion of diseased conspecifics) practiced by Caribbean spiny lobsters (Panulirus argus) when subject to the socially transmitted PaV1 virus, appears to have prevented an epizootic over a large seascape. We capitalized on a natural experiment in which a die-off of sponges in the Florida Keys (USA) resulted in a loss of shelters for juvenile lobsters over a similar to 2500km(2) region. Lobsters were thus concentrated in the few remaining shelters, presumably increasing their exposure to the contagious virus. Despite this spatial reorganization of the population, viral prevalence in lobsters remained unchanged after the sponge die-off and for years thereafter. A field experiment in which we introduced either a healthy or PaV1-infected lobster into lobster aggregations in natural dens confirmed that spiny lobsters practice behavioral immunity. Healthy lobsters vacated dens occupied by PaV1-infected lobsters despite the scarcity of alternative shelters and the higher risk of predation they faced when searching for a new den. Simulations from a spatially-explicit, individual-based model confirmed our empirical results, demonstrating the efficacy of behavioral immunity in preventing epizootics in this system

Aquatic polymers can drive pathogen transmission in coastal ecosystems.

Gelatinous polymers including extracellular polymeric substances (EPSs) are fundamental to biophysical processes in aquatic habitats, including mediating aggregation processes and functioning as the matrix of biofilms. Yet insight into the impact of these sticky molecules on the environmental transmission of pathogens in the ocean is limited. We used the zoonotic parasite Toxoplasma gondii as a model to evaluate polymer-mediated mechanisms that promote transmission of terrestrially derived pathogens to marine fauna and humans. We show that transparent exopolymer particles, a particulate form of EPS, enhance T. gondii association with marine aggregates, material consumed by organisms otherwise unable to access micrometre-sized particles. Adhesion to EPS biofilms on macroalgae also captures T. gondii from the water, enabling uptake of pathogens by invertebrates that feed on kelp surfaces. We demonstrate the acquisition, concentration and retention of T. gondii by kelp-grazing snails, which can transmit T. gondii to threatened California sea otters. Results highlight novel mechanisms whereby aquatic polymers facilitate incorporation of pathogens into food webs via association with particle aggregates and biofilms. Identifying the critical role of invisible polymers in transmission of pathogens in the ocean represents a fundamental advance in understanding and mitigating the health impacts of coastal habitat pollution with contaminated runoff

The Role of Scavenging in Disease Dynamics

Contents Introduction................ 161 The Use of Animal Remains and the Exposure of Scavengers to Disease........ 163 The Relevance of Scavenging for Pathogens to Spread and Persist.......... 166 Human Related Factors Resulting in Increased Risk for Disease Transmission Through Scavenging.............. 170 Management of Scavenging to Reduce Disease Risks.............. 173 Restoration of Large Predators.................. 174 Elimination of Hunting of Scavengers............ 174 Destruction of Big Game and Domestic Animal Carcasses........... 174 Restoration of the Effects of Overabundance............. 175 Excluding Mammalian and Avian Scavengers from Natural Carrions.......... 176 Excluding Mammalian and Avian Scavengers from Vulture Restaurants........... 176 Conclusions and Future Perspectives........... 178 References............... 17