Review
Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission

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Recent reviews have argued that disease control is among the ecosystem services yielded by biodiversity. Lyme disease (LD) is commonly cited as the best example of the ‘diluting’ effect of biodiversity on disease transmission, but many studies document the opposite relationship, showing that human LD risk can increase with forestation. Here, we unify these divergent perspectives and find strong evidence for a positive link between biodiversity and LD at broad spatial scales (urban to suburban to rural) and equivocal evidence for a negative link between biodiversity and LD at varying levels of biodiversity within forests. This finding suggests that, across zoonotic disease agents, the biodiversity–disease relationship is scale dependent and complex.

Section snippets

Can biodiversity protect humans against disease?

Does anthropogenic biodiversity loss generally increase or decrease zoonotic disease transmission? This is a contentious question in disease ecology, and its answer is not only of theoretical interest, but also reveals whether biodiversity conservation could be deployed as an effective approach for disease control. LD has become a major focus in this controversy. Understanding how to interrupt transmission of LD (which is caused by the spirochete pathogen Borrelia burgdorferi and vectored by

LD transmission

The complex transmission cycle of LD is now well known. The pathogen is a spirochete bacterium, B. burgdorferi, which is vectored by ixodid ticks. Although the ticks are generalized feeders and can take blood meals from many forest vertebrates, they tend to use small animals in their early life stages and large animals in the adult stage [26]. In the northeastern USA, many black-legged tick larvae and nymphs (Ixodes scapularis) feed on the white-footed mouse (Peromyscus leucopus), whereas the

An approach for reconciling divergent perspectives on the relationship of biodiversity to LD risk

Here, we outline the traditional and dilution effect perspectives, illustrate them with path diagrams (Figure 1) and transmission cycles (Figure 2), and place them in their historical context (Box 1). We then present a synthetic, cohesive framework for the dependence of human LD risk on biodiversity, with an emphasis on the importance of spatial resolution in understanding this relationship. We find strong evidence for a positive link between biodiversity and disease at broad spatial scales

The traditional perspective

Although the historical ecology of LD was not understood until years after the disease was first identified in 1977 (Box 1), links between LD and forests were widely recognized in the literature, even in the earliest days of the LD epidemic. In one of the first investigations of the ecology of LD and its hosts, Wallis et al. [28] wrote, ‘Patients have clustered in sparsely settled, often wooded, rural areas of southeastern Connecticut.’ When ecologists and epidemiologists set out to assess

The dilution effect perspective

In 2000 and 2001, several papers 13, 36, 37 proposed a different view of LD transmission. Called the ‘dilution effect’, the new hypothesis argued that high biodiversity could actually protect humans from LD and other infectious diseases. Here, we use the inclusive definition of the dilution effect 19, 38, which refers to scenarios in which biodiversity provides the ecosystem service of disease reduction. The dilution effect hypothesis has three important assumptions: (i) that reservoir hosts

Using spatial scale to reconcile divergent perspectives on biodiversity and LD risk

Aside from the scientific issues with the dilution effect studies outlined above, we suggest that the traditional and dilution effect perspectives lead to opposite predictions about the effect of forestation and/or biodiversity on LD risk because they focus on variation in risk at different spatial resolutions. Whereas studies of the dilution effect tend to compare LD risk among sites within forested areas, papers with an epidemiological focus have traditionally investigated LD risk across a

The importance of temporal scale in measuring response of LD risk to changes in biodiversity

One dynamic that models cannot easily consider is the potential effect of rapid changes in biodiversity on the density of questing ticks (i.e., ticks in search of a blood meal; [52]). If questing ticks do not find a suitable wild host, their abundance builds up, making encounters with humans more likely. This is best illustrated with the example of oak mast in the northeastern US forests where LD has been well studied. Oak acorn production is naturally variable, with oak trees synchronously

A unified perspective on the relationship of biodiversity to LD risk

Papers on LD have reached divergent conclusions because their different perspectives, although built on logical causal paths, are incomplete. Many recent studies have recognized the need to combine perspectives 9, 30, 33, 37, 38, 41, 48, 55, 56 (Figure 1c). The resulting synthesis is, by necessity, more complex. It has 12 paths from forestation and/or biodiversity to human health risk, including some paths with ambiguous signs. Due to the mixture of positive, negative, and ambiguous compound

Conservation and disease control

Reviews of the dilution effect have often cited LD as the principal evidence for the conclusion that biodiversity protects human populations against infectious disease (e.g., 16, 19, 21, 22, 23, 24, 25). This is part of a growing effort to market conservation actions based on the utilitarian services that biodiversity can provide for human society. Dilution is a logical outcome under some circumstances, particularly for short periods of time and at small spatial scales. It is understandable

Concluding remarks

Evidence or logical arguments support all the proposed paths in Figure 1c, but their relative strengths are unclear. Despite the uncertainty of the individual paths, the empirical evidence is most consistent with a positive indirect effect of forestation on LD risk in humans (Figure 2c). Spatial correlations between forested land and human LD cases have been demonstrated across the northeastern USA at a variety of scales and resolutions (e.g., 2, 3, 4, 5, 6, 7, 8, 9, 10). The only effective

Acknowledgments

C.L.W. was supported by a National Science Foundation Graduate Research Fellowship and an Alyce B. and Henry J. Ramey, Jr. Stanford Graduate Fellowship. Uriel Kitron, Dan Salkeld, Andrea Swei, and six anonymous reviewers made helpful comments on earlier versions of this manuscript.

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