Abstract Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock‐on effects, such as trophic cascades, on the wider ecosystem. While such indirect effects stemming from the fear of predation have received extensive attention for herbivore–plant and predator–prey interactions, much less is known about how they alter parasite–host interactions and wildlife diseases. In this synthesis, we present a conceptual framework for how predation risk—as perceived by organisms that serve as hosts—can affect parasite–host interactions, with implications for infectious disease dynamics. By basing our approach on recent conceptual advances with respect to predation risk effects, we aim to expand this general framework to include parasite–host interactions and diseases. We further identify pathways through which parasite–host interactions can be affected, for example, through altered parasite avoidance behavior or tolerance of hosts to infections, and discuss the wider relevance of predation risk for parasite and host populations, including heuristic projections to population‐level dynamics. Finally, we highlight the current unknowns, specifically the quantitative links from individual‐level processes to population dynamics and community structure, and emphasize approaches to address these knowledge gaps.
more »
« less
Individual variation underlies large‐scale patterns: Host conditions and behavior affect parasitism
Abstract Identifying the factors that affect host–parasite interactions is essential for understanding the ecology and dynamics of vector‐borne diseases and may be an important component of predicting human disease risk. Characteristics of hosts themselves (e.g., body condition, host behavior, immune defenses) may affect the likelihood of parasitism. However, despite highly variable rates of parasitism and infection in wild populations, identifying widespread links between individual characteristics and heterogeneity in parasite acquisition has proven challenging because many zoonoses exist over wide geographic extents and exhibit both spatial and temporal heterogeneity in prevalence and individual and population‐level effects. Using seven years of data collected by the National Ecological Observatory Network (NEON), we examined relationships among individual host condition, behavior, and parasitism byIxodidticks in a keystone host species, the white‐footed mouse,Peromyscus leucopus. We found that individual condition, specifically sex, body mass, and reproductive condition, had both direct and indirect effects on parasitism by ticks, but the nature of these effects differed for parasitism by larval versus nymphal ticks. We also found that condition differences influenced rodent behavior, and behavior directly affected the rates of parasitism, with individual mice that moved farther being more likely to carry ticks. This study illustrates how individual‐level data can be examined using large‐scale datasets to draw inference and uncover broad patterns in host–parasite encounters at unprecedented spatial scales. Our results suggest that intraspecific variation in the movement ecology of hosts may affect host–parasite encounter rates and, ultimately, alter zoonotic disease risk through anthropogenic modifications and natural environmental conditions that alter host space use.
more »
« less
- Award ID(s):
- 2110031
- PAR ID:
- 10588978
- Publisher / Repository:
- Ecological Society of America
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 106
- Issue:
- 1
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Understanding the community ecology of vector-borne and zoonotic diseases, and how it may shift transmission risk as it responds to environmental change, has become a central focus in disease ecology. Yet, it has been challenging to link the ecology of disease with reported human incidence. Here, we bridge the gap between local-scale community ecology and large-scale disease epidemiology, drawing from a priori knowledge of tick-pathogen-host ecology to model spatially-explicit Lyme disease (LD) risk, and human Lyme disease incidence (LDI) in California. We first use a species distribution modeling approach to model disease risk with variables capturing climate, vegetation, and ecology of key reservoir host species, and host species richness. We then use our modeled disease risk to predict human disease incidence at the zip code level across California. Our results suggest the ecology of key reservoir hosts—particularly dusky-footed woodrats—is central to disease risk posed by ticks, but that host community richness is not strongly associated with tick infection. Predicted disease risk, which is most strongly influenced by the ecology of dusky-footed woodrats, in turn is a strong predictor of human LDI. This relationship holds in the Wildland-Urban Interface, but not in open access public lands, and is stronger in northern California than in the state as a whole. This suggests peridomestic exposure to infected ticks may be more important to LD epidemiology in California than recreational exposure, and underlines the importance of the community ecology of LD in determining human transmission risk throughout this LD endemic region of far western North America. More targeted tick and pathogen surveillance, coupled with studies of human and tick behavior could improve understanding of key risk factors and inform public health interventions. Moreover, longitudinal surveillance data could further improve forecasts of disease risk in response to global environmental change.more » « less
-
Predators and parasites are critical, interconnected members of the community and have the potential to shape host populations. Predators, in particular, can have direct and indirect impacts on disease dynamics. By removing hosts and their parasites, predators alter both host and parasite populations and ultimately shape disease transmission. Selective predation of infected hosts has received considerable attention as it is recognized to have important ecological implications. The occurrence and consequences of preferential consumption of uninfected hosts, however, has rarely been considered. Here, we synthesize current evidence suggesting this strategy of selectively predating uninfected individuals is likely more common than previously anticipated and address how including this predation strategy can change our understanding of the ecology and evolution of disease dynamics. Selective predation strategies are expected to differentially impact ecological dynamics and therefore, consideration of both strategies is required to fully understand the impact of predation on prey and host densities. In addition, given that different strategies of prey selectivity by predators change the fitness payoffs both for hosts and their parasites, we predict amplified coevolutionary rates under selective predation of infected hosts compared to uninfected hosts. Using recent work highlighting the critical role that predators play in disease dynamics, we provide insights into the potential mechanisms by which selective predation on healthy individuals can directly affect ecological outcomes and impact long‐term host–parasite coevolution. We contrast the consequences of both scenarios of selective predation while identifying current gaps in the literature and future research directions.more » « less
-
Abstract Co‐parasitism is ubiquitous and has important consequences for the ecology and evolution of wild host populations. Studies of parasite co‐infections remain limited in scope, with few experimental tests of the fitness consequences of multiple parasites, especially in natural populations.We measured the separate and combined effects ofPhilornis seguyinest flies and shiny cowbirdsMolothrus bonariensison the fitness of a shared host, the chalk‐browed mockingbird (Mimus saturninus) in Argentina.Using a two‐factor experimental approach, we manipulated the presence of nest flies and cowbirds in mockingbird nests and assessed their effects on mockingbird haemoglobin levels, begging and provisioning rates, body size, and fledging success. We also monitored rates of nest predation in relation to parasitism by flies and cowbirds.Nest flies reduced the haemoglobin concentration, body size, and fledging success of mockingbirds, likely because mockingbirds did not compensate for parasitism by begging more or feeding their nestlings more. Cowbirds also reduced the fledging success of mockingbirds, even though they had no detectable effect on haemoglobin or body size. Nests with cowbirds, which beg more than mockingbirds, attracted more nest predators. There was no significant interaction between the effects of flies and cowbirds on any component of mockingbird fitness. The combined effects of nest flies and cowbirds were strictly additive.In summary, we show that nest flies and cowbirds both reduce host fitness, but do not have interactive effects in co‐parasitized nests. Our results further suggest that predators exacerbate the effects of nest flies and cowbirds on their hosts. Our study shows that the fitness consequences of co‐parasitism are complex, especially in the context of community‐level interactions.more » « less
-
Abstract Heterogeneous distributions are a fundamental principle of ecology, manifesting as natural variability within ecological levels of organization from individuals to ecosystems. In disease ecology, variability in biotic and abiotic factors can result in heterogeneous patterns of transmission and virulence—broadly defined here as the negative consequences of infection. Still, our classic theoretical understanding of disease dynamics comes from models that assume homogeneous transmission and virulence. Here, we test this assumption by assessing the contribution of various sources of individual and spatial heterogeneity to patterns of transmission and sublethal measurements of virulence in two lizard–malaria systems: a three‐parasite assemblage (Plasmodium floridense,Plasmodium leukocytica, andPlasmodium azurophilum) infecting the lizardAnolis gundlachiin the rainforest of Puerto Rico and a single‐parasite system (P. floridense–Anolis sagrei) in Florida. Using a Bayesian model selection framework, we evaluated whether individual host differences (i.e., body size and sex) or spatial variability (i.e., habitat type and local‐scale host spatial structure) drive heterogeneity in the probability of infection or its associated health costs (i.e., body condition, blood chemistry). We found that the probability of infection increases with increasing lizard body size in both systems. However, in Florida, we found the relationship to be subdued in deforested habitats compared to the adjacent urban hydric forests. Furthermore, infection was spatially clustered within sampling sites, with “hot” and “cold” spots across the landscape. Nevertheless, we found no clear evidence of costs of infection on lizard health in any of the measures assessed and hence no grounds for inference regarding heterogeneous virulence. Ultimately, the consistency of our results across systems suggests prominent roles of individual and spatial heterogeneities as driving factors of transmission of vector‐borne diseases.more » « less
An official website of the United States government

