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. 2017 Jun 5;372(1722):20160173.
doi: 10.1098/rstb.2016.0173.

Null expectations for disease dynamics in shrinking habitat: dilution or amplification?

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Null expectations for disease dynamics in shrinking habitat: dilution or amplification?

Christina L Faust et al. Philos Trans R Soc Lond B Biol Sci. .

Abstract

As biodiversity declines with anthropogenic land-use change, it is increasingly important to understand how changing biodiversity affects infectious disease risk. The dilution effect hypothesis, which points to decreases in biodiversity as critical to an increase in infection risk, has received considerable attention due to the allure of a win-win scenario for conservation and human well-being. Yet some empirical data suggest that the dilution effect is not a generalizable phenomenon. We explore the response of pathogen transmission dynamics to changes in biodiversity that are driven by habitat loss using an allometrically scaled multi-host model. With this model, we show that declining habitat, and thus declining biodiversity, can lead to either increasing or decreasing infectious-disease risk, measured as endemic prevalence. Whether larger habitats, and thus greater biodiversity, lead to a decrease (dilution effect) or increase (amplification effect) in infection prevalence depends upon the pathogen transmission mode and how host competence scales with body size. Dilution effects were detected for most frequency-transmitted pathogens and amplification effects were detected for density-dependent pathogens. Amplification effects were also observed over a particular range of habitat loss in frequency-dependent pathogens when we assumed that host competence was greatest in large-bodied species. By contrast, only amplification effects were observed for density-dependent pathogens; host competency only affected the magnitude of the effect. These models can be used to guide future empirical studies of biodiversity-disease relationships across gradients of habitat loss. The type of transmission, the relationship between host competence and community assembly, the identity of hosts contributing to transmission, and how transmission scales with area are essential factors to consider when elucidating the mechanisms driving disease risk in shrinking habitat.This article is part of the themed issue 'Conservation, biodiversity and infectious disease: scientific evidence and policy implications'.

Keywords: allometry; amplification effect; dilution effect; disease ecology; habitat loss; infectious disease dynamics; multi-host.

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Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.
Community disease prevalence in a shrinking habitat. Each row represents a unique community assemblage assumption—figures in column 1 indicate when a species is present in a habitat patch of a given size, and the shade indicates modifications to density (lighter = less dense/lower ɛia; see methods and SI for details). The prevalence of infection in individual species and the overall community at equilibrium (t = 150 years) in both frequency-dependent (column 2) and density-dependent (column 3) transmission simulations are shown. There was no variation in host competence or between-species contact (within-species R0 = 2.0; ψ = 0.5). Simulations for a single community, shown in colour, represent a community with species that have an average mass of 0.011, 0.030, 0.065, 0.075, 0.23, 0.537, 1.505, 1.515, 13.333, 14.201 kg. For all simulations, the prevalence for each species is shown with colours representing their size, from brown (smallest host) to aquamarine (largest host). The black line indicates the prevalence of disease across the community and is most similar to the intermediate body classes. Simulations with 100 random communities are shown in electronic supplementary material, figure S7. A pathogen with frequency-dependent transmission declines in prevalence as habitat area increases (from left to right) and species richness increases, thus leading to a dilution effect, although the strength of this declines with increasing randomness in the community structure. Pathogen prevalence within each species and across the entire population increased as habitat size increased for density-dependent pathogens, demonstrating an amplification effect; however, this asymptotes when species were no longer added to the community. Community assembly only affects the rate of increase or decrease in prevalence when species and abundance are nested, but not the directionality of diversity–disease relationships. When species presence and density are not directly related to area, then the relationship between diversity and disease becomes less predictable.
Figure 2.
Figure 2.
Variation in host competence and underlying assumptions impact diversity–disease relationships. (a) Even if the smallest hosts are the most competent [61] and there are extreme differences in R0 between body sizes (electronic supplementary material, figure S5), only the amplification effect is observed for density-dependent pathogens. (b) If behavioural allometry leads to an increase in R0 across body size, this can lead to an amplification effect for frequency-dependent pathogens at larger patch sizes, but a dilution effect for small to intermediate patches. (c) When species that can become infected but are in turn not infectious (incompetent hosts, denoted by x) are randomly assembled along the distribution of body sizes, then dilution effects can be exacerbated for frequency-dependent pathogens, but this depends on the order of community introduction of these incompetent hosts.
Figure 3.
Figure 3.
Impact of heterogeneous contacts on density-dependent pathogen transmission. Using identical disease parameters, endemic prevalence was observed for a host system that assumed contacts were determined by density of hosts (a) and compared with a system in which home range determined the average contacts of an individual from a given species (b). When home range is not taken into account, overall prevalence is higher, but when home range is considered, larger-bodied species that have larger home ranges have higher within-species infection prevalence.

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