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 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.     

Evolution of parasite virulence when host responses cause disease

The trade-off hypothesis of virulence evolution rests on the assumption that infection-induced mortality is a consequence of host exploitation by parasites. This hypothesis lies at the heart of many empirical and theoretical studies of virulence evolution, despite growing evidence that infection-induced mortality is very often a by-product of host immune responses. We extend the theoretical framework of the trade-off hypothesis to incorporate such immunopathology and explore how this detrimental aspect of host defence mechanisms affects the evolution of pathogen exploitation and hence infection-induced mortality. We argue that there are qualitatively different ways in which immunopathology can arise and suggest ways in which empirical studies can tease apart these effects. We show that immunopathology can cause infection-induced mortality to increase or decrease as a result of pathogen evolution, depending on how it covaries with pathogen exploitation strategies and with parasite killing by hosts. Immunopathology is thus an important determinant of whether public and animal health programmes will drive evolution in a clinically beneficial or detrimental direction. Immunopathology complicates our understanding of disease evolution, but can nevertheless be readily accounted for within the framework of the trade-off hypothesis.     

Landscape-level toxicant exposure mediates infection impacts on wildlife populations

Anthropogenic landscape modification such as urbanization can expose wildlife to toxicants, with profound behavioural and health effects. Toxicant exposure can alter the local transmission of wildlife diseases by reducing survival or altering immune defence. However, predicting the impacts of pathogens on wildlife across their ranges is complicated by heterogeneity in toxicant exposure across the landscape, especially if toxicants alter wildlife movement from toxicant-contaminated to uncontaminated habitats. We developed a mechanistic model to explore how toxicant effects on host health and movement propensity influence range-wide pathogen transmission, and zoonotic exposure risk, as an increasing fraction of the landscape is toxicant-contaminated. When toxicant-contaminated habitat is scarce on the landscape, costs to movement and survival from toxicant exposure can trap infected animals in contaminated habitat and reduce landscape-level transmission. Increasing the proportion of contaminated habitat causes host population declines from combined effects of toxicants and infection. The onset of host declines precedes an increase in the density of infected hosts in contaminated habitat and thus may serve as an early warning of increasing potential for zoonotic spillover in urbanizing landscapes. These results highlight how sublethal effects of toxicants can determine pathogen impacts on wildlife populations that may not manifest until landscape contamination is widespread.     

Heterogeneity in patch quality buffers metapopulations from pathogen impacts

Many wildlife species persist on a network of ephemerally occupied habitat patches connected by dispersal. Provisioning of food and other resources for conservation management or recreation is frequently used to improve local habitat quality and attract wildlife. Resource improvement can also facilitate local pathogen transmission, but the landscape-level consequences of provisioning for pathogen spread and habitat occupancy are poorly understood. Here, we develop a simple metapopulation model to investigate how heterogeneity in patch quality resulting from resource improvement influences long-term metapopulation occupancy in the presence of a virulent pathogen. We derive expressions for equilibrium host–pathogen outcomes in terms of provisioning effects on individual patches (through decreased patch extinction rates) and at the landscape level (the fraction of high-quality, provisioned patches), and highlight two cases of practical concern. First, if occupancy in the unprovisioned metapopulation is sufficiently low, a local maximum in occupancy occurs for mixtures of high- and low-quality patches, such that further increasing the number of high-quality patches both lowers occupancy and allows pathogen invasion. Second, if the pathogen persists in the unprovisioned metapopulation, further provisioning can result in all patches becoming infected and in a global minimum in occupancy. This work highlights the need for more empirical research on landscape-level impacts of local resource provisioning on pathogen dynamics.     

Host condition as a constraint for parasite reproduction

Environmental stress has been suggested to increase host susceptibility to infections and reduce host ability to resist parasite growth and reproduction, thus benefiting parasites. This prediction stems from expected costs of immune defence; hosts in poor condition should have less resources to be allocated to immune function. However, the alternative hypothesis for response to environmental stress is that hosts in poor condition provide less resources for parasites and/or suffer higher mortality, leading to reduced parasite growth, reproduction and survival. We contrasted these alternative hypotheses in a trematode–snail ( Diplostomum spathaceum – Lymnaea stagnalis ) system by asking: (1) how host condition affects parasite reproduction (amount and quality of produced transmission stages) and (2) how host condition affects the survival of infected host individuals. We experimentally manipulated host condition by starving the snails, and found that parasites produced fewer and poorer quality transmission stages in stressed hosts. Furthermore, starvation increased snail mortality. These findings indicate that in well-established trematode infections, reduced ability of immune allocation has no effect on host exploitation by parasites. Instead, deteriorating resources for the snail host can directly limit the amount of resources available for the parasite. This, together with increased host mortality, may have negative effects on parasite populations in the wild.     

Knock‐on community impacts of a novel vector: spillover of emerging DWV‐B from Varroa‐infested honeybees to wild bumblebees

Novel transmission routes can directly impact the evolutionary ecology of infectious diseases, with potentially dramatic effect on host populations and knock‐on effects on the wider host community. The invasion of Varroa destructor, an ectoparasitic viral vector in Western honeybees, provides a unique opportunity to examine how a novel vector affects disease epidemiology in a host community. This specialist honeybee mite vectors deformed wing virus (DWV), an important re‐emerging honeybee pathogen that also infects wild bumblebees. Comparing island honeybee and wild bumblebee populations with and without V. destructor, we show that V. destructor drives DWV prevalence and titre in honeybees and sympatric bumblebees. Viral genotypes are shared across hosts, with the potentially more virulent DWV‐B overtaking DWV‐A in prevalence in a current epidemic. This demonstrates disease emergence across a host community driven by the acquisition of a specialist novel transmission route in one host, with dramatic community level knock‐on effects.     

Galapagos ground finches balance investment in behavioural and immunological pathogen defences

The scientific community has long recognized the importance of individual behaviour in pathogen spread in wild animals. Furthermore, recent studies have highlighted the potential for behaviour to act as a pathogen defence mechanism. In line with these studies, the pathogen defence optimization hypothesis (PDOH) posits that individuals balance investment in costly behavioural and immunological defences against pathogen infection. Here, I test the PDOH using data from observations of wild Galapagos finches (Medium Ground Finches Geospiza fortis and Small Ground Finches Geospiza fuliginosa) at feeders, combined with immune data collected in the field. Both within and between species, those groups engaging to a greater extent in high transmission‐risk behaviours (not investing in behavioural defences against pathogen exposure) invest more heavily in immune pathogen defences. These data provide the first support for the PDOH in a wild population.     

Food provisioning alters infection dynamics in populations of a wild rodent

While pathogens are often assumed to limit the growth of wildlife populations, experimental evidence for their effects is rare. A lack of food resources has been suggested to enhance the negative effects of pathogen infection on host populations, but this theory has received little investigation. We conducted a replicated two-factor enclosure experiment, with introduction of the bacterium Bordetella bronchiseptica and food supplementation, to evaluate the individual and interactive effects of pathogen infection and food availability on vole populations during a boreal winter. We show that prior to bacteria introduction, vole populations were limited by food availability. Bordetella bronchiseptica introduction then reduced population growth and abundance, but contrary to predictions, primarily in food supplemented populations. Infection prevalence and pathological changes in vole lungs were most common in food supplemented populations, and are likely to have resulted from increased congregation and bacteria transmission around feeding stations. Bordetella bronchiseptica-infected lungs often showed protozoan co-infection (consistent with Hepatozoon erhardovae), together with more severe inflammatory changes. Using a multidisciplinary approach, this study demonstrates a complex picture of interactions and underlying mechanisms, leading to population-level effects. Our results highlight the potential for food provisioning to markedly influence disease processes in wildlife mammal populations.     

An island paradigm on the mainland: host population fragmentation impairs the community of avian pathogens

Emergent infectious diseases represent a major threat for biodiversity in fragmented habitat networks, but their dynamics in host metapopulations remain largely unexplored. We studied a large community of pathogens (including 26 haematozoans, bacteria and viruses as determined through polymerase chain reaction assays) in a highly fragmented mainland bird metapopulation. Contrary to recent studies, which have established that the prevalence of pathogens increase with habitat fragmentation owing to crowding and habitat-edge effects, the analysed pathogen parameters were neither dependent on host densities nor related to the spatial structure of the metapopulation. We provide, to our knowledge, the first empirical evidence for a positive effect of host population size on pathogen prevalence, richness and diversity. These new insights into the interplay between habitat fragmentation and pathogens reveal properties of a host-pathogen system resembling island environments, suggesting that severe habitat loss and fragmentation could lower pathogen pressure in small populations.     

Modelling Parasite Transmission in a Grazing System: The Importance of Host Behaviour and Immunity

Parasitic helminths present one of the most pervasive challenges to grazing herbivores. Many macro-parasite transmission models focus on host physiological defence strategies, omitting more complex interactions between hosts and their environments. This work represents the first model that integrates both the behavioural and physiological elements of gastro-intestinal nematode transmission dynamics in a managed grazing system. A spatially explicit, individual-based, stochastic model is developed, that incorporates both the hosts’ immunological responses to parasitism, and key grazing behaviours including faecal avoidance. The results demonstrate that grazing behaviour affects both the timing and intensity of parasite outbreaks, through generating spatial heterogeneity in parasite risk and nutritional resources, and changing the timing of exposure to the parasites’ free-living stages. The influence of grazing behaviour varies with the host-parasite combination, dependent on the development times of different parasite species and variations in host immune response. Our outputs include the counterintuitive finding that under certain conditions perceived parasite avoidance behaviours (faecal avoidance) can increase parasite risk, for certain host-parasite combinations. Through incorporating the two-way interaction between infection dynamics and grazing behaviour, the potential benefits of parasite-induced anorexia are also demonstrated. Hosts with phenotypic plasticity in grazing behaviour, that make grazing decisions dependent on current parasite burden, can reduce infection with minimal loss of intake over the grazing season. This paper explores how both host behaviours and immunity influence macro-parasite transmission in a spatially and temporally heterogeneous environment. The magnitude and timing of parasite outbreaks is influenced by host immunity and behaviour, and the interactions between them; the incorporation of both regulatory processes is required to fully understand transmission dynamics. Understanding of both physiological and behavioural defence strategies will aid the development of novel approaches for control.     

Deposition of pathogenic Mycoplasma gallisepticum onto bird feeders: host pathology is more important than temperature-driven increases in food intake

Although ambient temperature has diverse effects on disease dynamics, few studies have examined how temperature alters pathogen transmission by changing host physiology or behaviour. Here, we test whether reducing ambient temperature alters host foraging, pathology and the potential for fomite transmission of the bacterial pathogen Mycoplasma gallisepticum (MG), which causes seasonal outbreaks of severe conjunctivitis in house finches (Haemorhous mexicanus). We housed finches at temperatures within or below the thermoneutral zone to manipulate food intake by altering energetic requirements of thermoregulation. We predicted that pathogen deposition on bird feeders would increase with temperature-driven increases in food intake and with conjunctival pathology. As expected, housing birds below the thermoneutral zone increased food consumption. Despite this difference, pathogen deposition on feeders did not vary across temperature treatments. However, pathogen deposition increased with conjunctival pathology, independently of temperature and pathogen load, suggesting that MG could enhance its transmission by increasing virulence. Our results suggest that in this system, host physiological responses are more important for transmission potential than temperature-dependent alterations in feeding. Understanding such behavioural and physiological contributions to disease transmission is critical to linking individual responses to climate with population-level disease dynamics.     

Impact of life stage specific immune priming on invertebrate disease dynamics

The immune response of a host can have important impacts on host‐pathogen interactions, but investment in immunity often changes dynamically across the life history of a host. One form of investment involves the induction of a primed immune response against previously encountered pathogens that protects the host from re‐infection. In addition to providing immediate protective effects, immune priming can also provide two types of ‘delayed’ protection against pathogens: priming across life stages (ontogenic priming) and priming across generations (trans‐generational priming). Consequently both types of immune priming have the potential to mediate life history variability in host–pathogen interactions, which could have important consequences for disease prevalence and dynamics as well as for the demographic structure of the host population. Here we develop a stage‐structured SIRS model for an invertebrate host to explore the relative and combined impact of ontogenic priming and trans‐generational priming on infection prevalence, host population size, and population age structure. Our model predicts that both types of immune priming can dramatically reduce disease prevalence at equilibrium, but their individual and combined effects on population size and age structure depend on the magnitude of tradeoffs between immune protection and reproduction as well as on the symmetry of infection parameters between life stages. This model underscores the potential importance of life‐history based immune investment patterns for disease dynamics and highlights the need for wide‐spread empirical estimation of parameters that represent the maintenance of immune priming in insects.     

Allocation to sexual versus nonsexual disease transmission

Many diseases have both sexual and nonsexual transmission routes, and closely related diseases often differ in their degree of sexual transmission. We investigate the evolution of transmission mode as a function of host social and mating structure using a model in which disease transmission is explicitly dependent on the numbers of sexual and nonsexual contacts (which are themselves a function of population density) and per-contact infection probabilities. Most generally, and in the absence of trade-offs between the degree of sexual transmission and effects on host fecundity and mortality, nonsexual transmission is favored above the social-sexual crossover point (the host density at which the number of nonsexual contacts exceeds the number of sexual contacts), while sexual transmission is favored below this point. When changes in allocation to the two transmission modes are accompanied by changes in mortality or fecundity, both mixed and pure transmission strategies can be favored. If invading genotypes differ substantially from resident genotypes, genetic polymorphism in transmission mode is possible. The evolutionary outcomes are predictable from a knowledge of the equilibrium population sizes in relation to the social-sexual crossover point. Our results also show that predictions about dynamic outcomes, based on rates of invasion for single pathogens into healthy populations, do not adequately describe the resulting disease prevalence nor predict the subsequent evolutionary dynamics; once invasion of a pathogen has occurred, the conditions for spread of a second pathogen are themselves altered. If the host is considered as a single resource, our results show that two pathogens may coexist on a single resource if they use that resource differentially and have differential feedbacks on resource abundance; such resource feedback effects may be present in other biological systems.     

Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs

Predicting how climate change will affect disease dynamics requires an understanding of how the environment affects host–pathogen interactions. For amphibians, global declines and extinctions have been linked to a pathogenic chytrid fungus, Batrachochytrium dendrobatidis. Using a combination of body temperature measurements and disease assays conducted before and after the arrival of B. dendrobatidis, this study tested the hypothesis that body temperature affects the prevalence of infection in a wild population of Panamanian golden frogs (Atelopus zeteki). The timing of first detection of the fungus was consistent with that of a wave of epidemic infections spreading south and eastward through Central America. During the epidemic, many golden frogs modified their thermoregulatory behaviour, raising body temperatures above their normal set point. Odds of infection decreased with increasing body temperature, demonstrating that even slight environmental or behavioural changes have the potential to affect an individual''s vulnerability to infection. The thermal dependency of the relationship between B. dendrobatidis and its amphibian hosts demonstrates how the progression of an epidemic can be influenced by complex interactions between host and pathogen phenotypes and the environments in which they are found.     

Effects of species diversity on disease risk

The transmission of infectious diseases is an inherently ecological process involving interactions among at least two, and often many, species. Not surprisingly, then, the species diversity of ecological communities can potentially affect the prevalence of infectious diseases. Although a number of studies have now identified effects of diversity on disease prevalence, the mechanisms underlying these effects remain unclear in many cases. Starting with simple epidemiological models, we describe a suite of mechanisms through which diversity could increase or decrease disease risk, and illustrate the potential applicability of these mechanisms for both vector-borne and non-vector-borne diseases, and for both specialist and generalist pathogens. We review examples of how these mechanisms may operate in specific disease systems. Because the effects of diversity on multi-host disease systems have been the subject of much recent research and controversy, we describe several recent efforts to delineate under what general conditions host diversity should increase or decrease disease prevalence, and illustrate these with examples. Both models and literature reviews suggest that high host diversity is more likely to decrease than increase disease risk. Reduced disease risk with increasing host diversity is especially likely when pathogen transmission is frequency-dependent, and when pathogen transmission is greater within species than between species, particularly when the most competent hosts are also relatively abundant and widespread. We conclude by identifying focal areas for future research, including (1) describing patterns of change in disease risk with changing diversity; (2) identifying the mechanisms responsible for observed changes in risk; (3) clarifying additional mechanisms in a wider range of epidemiological models; and (4) experimentally manipulating disease systems to assess the impact of proposed mechanisms.     

Ecosystem dynamics, biological diversity and emerging infectious diseases

In this article, we summarize the major scientific developments of the last decade on the transmission of infectious agents in multi-host systems. Almost sixty percent of the pathogens that have emerged in humans during the last 30-40 years are of animal origin and about sixty percent of them show an important variety of host species besides humans (3 or more possible host species). In this review, we focus on zoonotic infections with vector-borne transmission and dissect the contrasting effects that a multiplicity of host reservoirs and vectors can have on their disease dynamics. We discuss the effects exerted by host and vector species richness and composition on pathogen prevalence (i.e., reduction, including the dilution effect, or amplification). We emphasize that, in multiple host systems and for vector-borne zoonotic pathogens, host reservoir species and vector species can exert contrasting effect locally. The outcome on disease dynamics (reduced pathogen prevalence in vectors when the host reservoir species is rich and increased pathogen prevalence when the vector species richness increases) may be highly heterogeneous in both space and time. We then ask briefly how a shift towards a more systemic perspective in the study of emerging infectious diseases, which are driven by a multiplicity of hosts, may stimulate further research developments. Finally, we propose some research avenues that take better into account the multi-host species reality in the transmission of the most important emerging infectious diseases, and, particularly, suggest, as a possible orientation, the careful assessment of the life-history characteristics of hosts and vectors in a community ecology-based perspective.     

Avian malaria infection intensity influences mosquito feeding patterns

Pathogen-induced host phenotypic changes are widespread phenomena that can dramatically influence host–vector interactions. Enhanced vector attraction to infected hosts has been reported in a variety of host–pathogen systems, and has given rise to the parasite manipulation hypothesis whereby pathogens may adaptively modify host phenotypes to increase transmission from host to host. However, host phenotypic changes do not always favour the transmission of pathogens, as random host choice, reduced host attractiveness and even host avoidance after infection have also been reported. Thus, the effects of hosts’ parasitic infections on vector feeding behaviour and on the likelihood of parasite transmission remain unclear. Here, we experimentally tested how host infection status and infection intensity with avian Plasmodium affect mosquito feeding patterns in house sparrows (Passer domesticus). In separate experiments, mosquitoes were allowed to bite pairs containing (i) one infected and one uninfected bird and (ii) two infected birds, one of which treated with the antimalarial drug, primaquine. We found that mosquitoes fed randomly when exposed to both infected and uninfected birds. However, when mosquitoes were exposed only to infected individuals, they preferred to bite the non-treated birds. These results suggest that the malarial parasite load rather than the infection itself plays a key role in mosquito attraction. Our findings partially support the parasite manipulation hypothesis, which probably operates via a reduction in defensive behaviour, and highlights the importance of considering parasite load in studies on host–vector–pathogen interactions.     

Infectious diseases of marine molluscs and host responses as revealed by genomic tools

More and more infectious diseases affect marine molluscs. Some diseases have impacted commercial species including MSX and Dermo of the eastern oyster, QPX of hard clams, withering syndrome of abalone and ostreid herpesvirus 1 (OsHV-1) infections of many molluscs. Although the exact transmission mechanisms are not well understood, human activities and associated environmental changes often correlate with increased disease prevalence. For instance, hatcheries and large-scale aquaculture create high host densities, which, along with increasing ocean temperature, might have contributed to OsHV-1 epizootics in scallops and oysters. A key to understanding linkages between the environment and disease is to understand how the environment affects the host immune system. Although we might be tempted to downplay the role of immunity in invertebrates, recent advances in genomics have provided insights into host and parasite genomes and revealed surprisingly sophisticated innate immune systems in molluscs. All major innate immune pathways are found in molluscs with many immune receptors, regulators and effectors expanded. The expanded gene families provide great diversity and complexity in innate immune response, which may be key to mollusc''s defence against diverse pathogens in the absence of adaptive immunity. Further advances in host and parasite genomics should improve our understanding of genetic variation in parasite virulence and host disease resistance.     

Interaction of <Emphasis Type="Italic">Candida albicans</Emphasis> with host cells: virulence factors,host defense,escape strategies,and the microbiota

The interaction between Candida albicans and its host cells is characterized by a complex interplay between the expression of fungal virulence factors, which results in adherence, invasion and cell damage, and the host immune system, which responds by secreting proinflammatory cytokines, activating antimicrobial activities and killing the fungal pathogen. In this review we describe this interplay by taking a closer look at how C. albicans pathogenicity is induced and executed, how the host responds in order to prevent and clear an infection, and which mechanisms C. albicans has evolved to bypass these immune responses to avoid clearance. Furthermore, we review studies that show how the presence of other microorganisms affects this interplay.     

The role of nutrition in viral disease

Malnutrition has been associated with a decrease in immune function. Impairment of immune function may lead to increased susceptibility to infection with viruses. Although there are many studies documenting the effect of host nutritional status on immune functions, fewer studies have examined the effect of host nutritional status on viral pathogenesis. This review examines the relationship between viral infection and the nutritional status of the host, and documents that not only can the nutritional status of the host affect immune function, but can have profound effects on the virus itself. One mechanism by which nutritional status affects the virulence of the viral pathogen involves selection for virulent viral genotypes. Other mechanisms remain to be elucidated.