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

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'.

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Diversifying forest communities may change Lyme disease risk: extra dimension to the dilution effect in Europe

Parasitology ◽

10.1017/s0031182016000688 ◽

2016 ◽

Vol 143 (10) ◽

pp. 1310-1319 ◽

Cited By ~ 15

Author(s):

SANNE C. RUYTS ◽

EVY AMPOORTER ◽

ELENA C. COIPAN ◽

LANDER BAETEN ◽

DIETER HEYLEN ◽

...

Keyword(s):

North America ◽

Lyme Disease ◽

Borrelia Burgdorferi ◽

Disease Risk ◽

Severe Disease ◽

Dilution Effect ◽

Ixodid Ticks ◽

Infection Prevalence ◽

Host Diversity ◽

Pine Stands

SUMMARYLyme disease is caused by bacteria of theBorrelia burgdorferigenospecies complex and transmitted by Ixodid ticks. In North America only one pathogenic genospecies occurs, in Europe there are several. According to the dilution effect hypothesis (DEH), formulated in North America, nymphal infection prevalence (NIP) decreases with increasing host diversity since host species differ in transmission potential. We analysedBorreliainfection in nymphs from 94 forest stands in Belgium, which are part of a diversification gradient with a supposedly related increasing host diversity: from pine stands without to oak stands with a shrub layer. We expected changing tree species and forest structure to increase host diversity and decrease NIP. In contrast with the DEH, NIP did not differ between different forest types. Genospecies diversity however, and presumably also host diversity, was higher in oak than in pine stands. Infected nymphs tended to harbourBorrelia afzeliiinfection more often in pine stands whileBorrelia gariniiandBorrelia burgdorferiss. infection appeared to be more prevalent in oak stands. This has important health consequences, since the latter two cause more severe disease manifestations. We show that the DEH must be nuanced for Europe and should consider the response of multiple pathogenic genospecies.

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A Candide response to Panglossian accusations by Randolph and Dobson: biodiversity buffers disease

Parasitology ◽

10.1017/s0031182013000541 ◽

2013 ◽

Vol 140 (10) ◽

pp. 1196-1198 ◽

Cited By ~ 25

Author(s):

RICHARD S. OSTFELD

Keyword(s):

Infectious Disease ◽

Disease Risk ◽

Negative Relationship ◽

Dilution Effect ◽

Widespread Phenomenon ◽

High Diversity

SUMMARYRandolph and Dobson (2012) criticize the dilution effect, which describes the negative relationship between biodiversity and infectious disease risk. Unfortunately, their commentary includes distortions, errors of omission, and errors of commission, which are rebutted herein. Contrary to their claims, the dilution effect is not a ‘mantra’ that asserts that reduced disease risk is a ‘universal’ outcome of high diversity. Although universality of the dilution effect has not been claimed, and conditions under which diversity can amplify disease risk have been described, the growing literature indicates that the dilution effect is indeed a widespread phenomenon.

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Conservation of biodiversity as a strategy for improving human health and well-being

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0131 ◽

2017 ◽

Vol 372 (1722) ◽

pp. 20160131 ◽

Cited By ~ 41

Author(s):

A. Marm Kilpatrick ◽

Daniel J. Salkeld ◽

Georgia Titcomb ◽

Micah B. Hahn

Keyword(s):

Public Health ◽

Biodiversity Conservation ◽

Disease Ecology ◽

Current Knowledge ◽

Public Health Intervention ◽

Well Being ◽

Pathogen Transmission ◽

Policy Implications ◽

Anthropogenic Processes ◽

Conservation Interventions

The Earth's ecosystems have been altered by anthropogenic processes, including land use, harvesting populations, species introductions and climate change. These anthropogenic processes greatly alter plant and animal communities, thereby changing transmission of the zoonotic pathogens they carry. Biodiversity conservation may be a potential win–win strategy for maintaining ecosystem health and protecting public health, yet the causal evidence to support this strategy is limited. Evaluating conservation as a viable public health intervention requires answering four questions: (i) Is there a general and causal relationship between biodiversity and pathogen transmission, and if so, which direction is it in? (ii) Does increased pathogen diversity with increased host biodiversity result in an increase in total disease burden? (iii) Do the net benefits of biodiversity conservation to human well-being outweigh the benefits that biodiversity-degrading activities, such as agriculture and resource utilization, provide? (iv) Are biodiversity conservation interventions cost-effective when compared to other options employed in standard public health approaches? Here, we summarize current knowledge on biodiversity–zoonotic disease relationships and outline a research plan to address the gaps in our understanding for each of these four questions. Developing practical and self-sustaining biodiversity conservation interventions will require significant investment in disease ecology research to determine when and where they will be effective. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’.

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Human infectious disease burdens decrease with urbanization but not with biodiversity

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0122 ◽

2017 ◽

Vol 372 (1722) ◽

pp. 20160122 ◽

Cited By ~ 43

Author(s):

Chelsea L. Wood ◽

Alex McInturff ◽

Hillary S. Young ◽

DoHyung Kim ◽

Kevin D. Lafferty

Keyword(s):

Infectious Disease ◽

Infectious Diseases ◽

Disease Transmission ◽

Scientific Evidence ◽

Dilution Effect ◽

Policy Implications ◽

Global Public Health ◽

Country Level ◽

Life Years ◽

Over Time

Infectious disease burdens vary from country to country and year to year due to ecological and economic drivers. Recently, Murray et al. (Murray CJ et al . 2012 Lancet 380 , 2197–2223. ( doi:10.1016/S0140-6736(12)61689-4 )) estimated country-level morbidity and mortality associated with a variety of factors, including infectious diseases, for the years 1990 and 2010. Unlike other databases that report disease prevalence or count outbreaks per country, Murray et al. report health impacts in per-person disability-adjusted life years (DALYs), allowing comparison across diseases with lethal and sublethal health effects. We investigated the spatial and temporal relationships between DALYs lost to infectious disease and potential demographic, economic, environmental and biotic drivers, for the 60 intermediate-sized countries where data were available and comparable. Most drivers had unique associations with each disease. For example, temperature was positively associated with some diseases and negatively associated with others, perhaps due to differences in disease agent thermal optima, transmission modes and host species identities. Biodiverse countries tended to have high disease burdens, consistent with the expectation that high diversity of potential hosts should support high disease transmission. Contrary to the dilution effect hypothesis, increases in biodiversity over time were not correlated with improvements in human health, and increases in forestation over time were actually associated with increased disease burden. Urbanization and wealth were associated with lower burdens for many diseases, a pattern that could arise from increased access to sanitation and healthcare in cities and increased investment in healthcare. The importance of urbanization and wealth helps to explain why most infectious diseases have become less burdensome over the past three decades, and points to possible levers for further progress in improving global public health. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’.

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Conservation, development and the management of infectious disease: avian influenza in China, 2004–2012

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0126 ◽

2017 ◽

Vol 372 (1722) ◽

pp. 20160126 ◽

Cited By ~ 3

Author(s):

Tong Wu ◽

Charles Perrings

Keyword(s):

Infectious Disease ◽

Risk Factors ◽

Avian Influenza ◽

Wildlife Conservation ◽

Disease Risk ◽

Risk Mitigation ◽

Scientific Evidence ◽

Migratory Bird ◽

Policy Implications ◽

Economic Risk

There is growing evidence that wildlife conservation measures have mixed effects on the emergence and spread of zoonotic disease. Wildlife conservation has been found to have both positive (dilution) and negative (contagion) effects. In the case of avian influenza H5N1 in China, the focus has been on negative effects. Lakes and wetlands attracting migrating waterfowl have been argued to be disease hotspots. We consider the implications of waterfowl conservation for H5N1 infections in both poultry and humans between 2004 and 2012. We model both environmental and economic risk factors. Environmental risk factors comprise the conditions that structure interaction between wild and domesticated birds. Economic risk factors comprise the cost of disease, biosecurity measures and disease risk mitigation. We find that H5N1 outbreaks in poultry populations are indeed sensitive to the existence of wild-domesticated bird mixing zones, but not in the way we would expect from the literature. We find that risk is decreasing in protected migratory bird habitat. Since the number of human cases is increasing in the number of poultry outbreaks, as expected, the implication is that the protection of wetlands important for migratory birds offers unexpected human health benefits. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’.

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The accelerated infectious disease risk in the Anthropocene: more outbreaks and wider global spread

10.1101/2020.04.20.049866 ◽

2020 ◽

Cited By ~ 2

Author(s):

Serge Morand ◽

Bruno A. Walther

Keyword(s):

Infectious Disease ◽

Economic Growth ◽

Disease Risk ◽

Disease Outbreaks ◽

Well Being ◽

Infectious Disease Outbreaks ◽

Disease Networks ◽

Increased Risk ◽

Climate Crisis ◽

Human Infectious Disease

The greatly accelerated economic growth during the Anthropocene has resulted in astonishing improvements in many aspects of human well-being, but has also caused the acceleration of risks, such as the interlinked biodiversity and climate crisis. Here, we report on another risk: the accelerated infectious disease risk associated with the number and geographic spread of human infectious disease outbreaks. Using the most complete, reliable, and up-to-date database on human infectious disease outbreaks (GIDEON), we show that the number of disease outbreaks, the number of diseases involved in these outbreaks, and the number of countries affected have increased during the entire Anthropocene. Furthermore, the spatial distribution of these outbreaks is becoming more globalized in the sense that the overall modularity of the disease networks across the globe has decreased, meaning disease outbreaks have become increasingly pandemic in their nature. This decrease in modularity is correlated with the increase in air traffic. We finally show that those countries and regions which are most central within these disease networks tend to be countries with higher GDPs. Therefore, one cost of increased global mobility and greater economic growth is the increased risk of disease outbreaks and their faster and wider spread. We briefly discuss three different scenarios which decision-makers might follow in light of our results.

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Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

10.21203/rs.3.rs-586674/v1 ◽

2021 ◽

Author(s):

Sara Louise Gandy ◽

Elizabeth Kilbride ◽

Roman Biek ◽

Caroline Millins ◽

Lucy Gilbert

Keyword(s):

Lyme Disease ◽

Disease Risk ◽

Dilution Effect ◽

High Density ◽

Infection Prevalence ◽

Vegetation Height ◽

Deer Density ◽

Pathogen Prevalence ◽

Tick Reproduction ◽

The Impact

Abstract Background: Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi s.l., the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure lowers vegetation which decreases rodent abundance thus reducing transmission (M3).Methods: In a large enclosure where red deer stags were kept at high density (32.5 deer/km²), we used an experimental design consisting of eight plots of 0.23ha, four being fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn and quantified vegetation height and density, and small mammal abundance Results: Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution (M2) and cascade (M3) mechanisms might outweigh the increased opportunities for transmission (M1). Presence of deer at high density led to lower vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher.Conclusion: High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing.

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Biodiversity series: The function of biodiversity in the ecology of vector-borne zoonotic diseases

Canadian Journal of Zoology ◽

10.1139/z00-172 ◽

2000 ◽

Vol 78 (12) ◽

pp. 2061-2078 ◽

Cited By ~ 213

Author(s):

Richard S Ostfeld ◽

Felicia Keesing

Keyword(s):

Species Diversity ◽

Lyme Disease ◽

Host Species ◽

Disease Risk ◽

Feeding Habits ◽

Dilution Effect ◽

Tick Population ◽

Infection Prevalence ◽

Vector Borne ◽

The Impact

This is a critical evaluation of the influence of species diversity within communities of vertebrates on the risk of human exposure to vector-borne zoonoses. Vertebrates serve as natural reservoirs of many disease agents (viral, bacterial, protozoal) that are transmitted to humans by blood-feeding arthropod vectors. We describe the natural history of the Lyme disease zoonosis to illustrate interactions among pathogens, vectors, vertebrate hosts, and risk to humans. We then describe how the presence of a diverse assemblage of vertebrates can dilute the impact of the principal reservoir (the white-footed mouse, Peromyscus leucopus) of Lyme disease spirochetes (Borrelia burgdorferi), thereby reducing the disease risk to humans. Exploring the logic of what we call the dilution effect reveals four conditions that are necessary for it to apply generally to vector-borne zoonoses: (1) the feeding habits of the vector are generalized; (2) the pathogen is acquired by the vector from hosts (as opposed to exclusively transovarial transmission); (3) reservoir competence (the ability of a particular host species to infect a vector) varies among host species; and (4) the most competent reservoir host tends to be a community dominant, as defined by the proportion of the tick population fed by that species. When these conditions are met, vertebrate communities with high species diversity will contain a greater proportion of incompetent reservoir hosts that deflect vector meals away from the most competent reservoirs, thereby reducing infection prevalence and disease risk. Incorporating the likelihood that the abundance of competent reservoirs is reduced in more diverse communities, owing to the presence of predators and competitors, reinforces the impact of the dilution effect on the density of infected vectors. A review of the literature reveals the generality, though not the universality, of these conditions, which suggests that the effects of diversity on disease risk may be widespread. Issues in need of further exploration include (i) the relative importance of diversity per se versus fluctuating numbers of particular species; (ii) the relevance of species richness versus evenness to the dilution effect; (iii) whether the dilution effect operates at both local and regional scales; and (iv) the shape of empirically determined curves relating diversity to measures of disease risk. Further studies linking community ecology with epidemiology are warranted.

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Host Richness Increases Tuberculosis Disease Risk in Game-Managed Areas

Microorganisms ◽

10.3390/microorganisms7060182 ◽

2019 ◽

Vol 7 (6) ◽

pp. 182 ◽

Cited By ~ 5

Author(s):

Jose Angel Barasona ◽

Christian Gortázar ◽

José de la Fuente ◽

Joaquín Vicente

Keyword(s):

Species Richness ◽

Host Species ◽

Life Histories ◽

Disease Risk ◽

Dilution Effect ◽

Pathogen Transmission ◽

Trade Offs ◽

Community Assemblages ◽

Animal Communities ◽

The Impact

Current scientific debate addresses whether species richness in animal communities may negatively moderate pathogen transmission and disease outcome (dilution effect), or to the contrary, if disease emergence benefits from more diverse community assemblages (amplification effect). The result may not depend exclusively on patterns of host species biodiversity but may depend on the specific composition of reservoir hosts and vectors, and their ecology. Host–pathogen interactions have shaped variations in parasite virulence, transmissibility and specificity. In the same way the importance of factors related to host exposure or to life history trade-offs are expected to vary. In this study, we demonstrate that ungulate host species richness correlates with increased community competence to maintain and transmit pathogens of the Mycobacterium tuberculosis complex (MTC) in game-managed areas in Mediterranean Spain. Therefore, we should consider natural and artificial variations in life histories of pathogens and host communities to characterize the impact of biodiversity on the health of diverse assemblages of human and animal communities. Since most approaches assessing epidemiology and transmission of shared pathogens only involve single- or pair-species, further research is needed to better understand the infection dynamics from complete community assemblages, at least in chronic diseases such as tuberculosis and in non-natural animal communities.

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Does the impact of biodiversity differ between emerging and endemic pathogens? The need to separate the concepts of hazard and risk

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0129 ◽

2017 ◽

Vol 372 (1722) ◽

pp. 20160129 ◽

Cited By ~ 25

Author(s):

Parviez R. Hosseini ◽

James N. Mills ◽

Anne-Hélène Prieur-Richard ◽

Vanessa O. Ezenwa ◽

Xavier Bailly ◽

...

Keyword(s):

Infectious Disease ◽

Disease Risk ◽

Scientific Evidence ◽

Policy Implications ◽

Pathogen Prevalence ◽

Interactive Relationship ◽

Hazard And Risk ◽

Disease Risks ◽

The Impact ◽

The Relationship

Biodiversity is of critical value to human societies, but recent evidence that biodiversity may mitigate infectious-disease risk has sparked controversy among researchers. The majority of work on this topic has focused on direct assessments of the relationship between biodiversity and endemic-pathogen prevalence, without disentangling intervening mechanisms; thus study outcomes often differ, fuelling more debate. Here, we suggest two critical changes to the approach researchers take to understanding relationships between infectious disease, both endemic and emerging, and biodiversity that may help clarify sources of controversy. First, the distinct concepts of hazards versus risks need to be separated to determine how biodiversity and its drivers may act differently on each. This distinction is particularly important since it illustrates that disease emergence drivers in humans could be quite different to the general relationship between biodiversity and transmission of endemic pathogens. Second, the interactive relationship among biodiversity, anthropogenic change and zoonotic disease risk, including both direct and indirect effects, needs to be recognized and accounted for. By carefully disentangling these interactions between humans' activities and pathogen circulation in wildlife, we suggest that conservation efforts could mitigate disease risks and hazards in novel ways that complement more typical disease control efforts. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’.

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