The Lyme Disease Debate

Host Biodiversity and Human Disease Risk

Sharon Levy

Disclosures

Environ Health Perspect. 2013;121(4):a120-a125. 

In This Article

Connecting the Dots

It makes intuitive sense that more Bb-resistant hosts in the wild should lower the risk of human infection. But nothing about Lyme disease is simple. It turns out that even a species completely immune to Lyme infection can amplify the risk for people.

It boils down to a numbers game. The tick population depends on the presence of hosts to provide blood meals. If a Bb-resistant host species feeds enough larval ticks to lower the density of infected nymphs at the next life stage, it's also likely to boost the overall tick population. That means more larvae will be around to feed on hosts that do pass along the disease, explains Randolph; the proportion of infected ticks may decline even as their abundance increases.

That phenomenon was illustrated in a recent experiment on Lyme disease ecology in California.[37] The western fence lizard is an important host for disease-bearing ticks there but is resistant to Bb. Its immune response to the bacterium is so powerful that a lizard can actually clear the infection from the midgut of ticks feeding on it.[38] This ability would seem to make the fence lizard the ultimate dilution host, and when researchers removed the lizards from test plots in oak woodlands, they expected the numbers of infected nymphal ticks to increase as a result. But the opposite occurred. The density of infected nymphs—and thus the potential risk of human infection—decreased in plots where lizards had been removed. The study, coauthored by Ostfeld, concluded that "the California Lyme disease system behaves differently than that in New York."

In a critique of what she calls the "biodiversity-buffers-disease paradigm," Randolph challenged the methodology and statistical analyses in Ostfeld's work.[39] She agrees that the dilution effect exists in nature, but she contends it is a rarity; depending on the circumstances in a given ecosystem, a greater diversity of vertebrate hosts may instead amplify the risk to humans. Furthermore, she says, it is not a simple changing index of biodiversity but specific changes in community structure that are critical to the outcome. Randolph is concerned that the dilution effect, shown to exist in a few specific situations for Lyme and other zoonotic diseases, is being used as an all-purpose argument for biodiversity conservation, which should be valued for other reasons. "The dilution effect is increasingly invoked but not well understood," she says.

Recent studies have attempted to track a dilution effect for an array of infectious diseases, including schistosomiasis, West Nile virus, malaria, and hantavirus pulmonary syndrome. Ostfeld, Keesing, and others have cited the dilution effect as an example of a win–win solution for conservation and public health.[40,41,42] Yet these authors acknowledge that the dilution effect doesn't always hold and that many zoonoses emerge from regions of high biodiversity.

There are some striking examples of a link between biodiversity loss and increased human disease risk. Schistosoma mansoni is a parasite of freshwater snails that reproduces inside its snail host. It also infects humans through skin contact with a free-swimming larval stage. When overfishing depleted the population of snail-eating cichlid fishes in Lake Malawi, the incidence of schistosomiasis there rose.[41,43] Experimental studies showed that adding snail species that resist the parasite lowered the infection rate in susceptible snails as well as the production of parasite larvae.[44]

However, this finding has not been tested in the field, and Chelsea Wood, a doctoral candidate in parasite and pathogen ecology at Stanford University, points out that schistosomiasis-infected snails don't reproduce; their trematode parasites castrate them. "Reducing the infection rate among snails temporarily reduces schistosomiasis risk but soon leads to increases in the abundance of snails because fewer snails are castrated," she explains. "The increased density of snails might lead to an increase in schistosomiasis risk, because even a small proportion of infections can mean a big risk if there are many snails." Wood is lead author on a recent review that synthesizes different perspectives on the ecology of Lyme disease.[7]

In the case of West Nile virus, birds are the primary hosts. The infection is spread by mosquito vectors, including Culex pipiens, a species well adapted to urban environments.[45] Some studies that examined human infection rates over broad geographic areas have found a correlation between increased diversity in bird communities and lowered rates of human infection.[46,47] But a study of bird diversity in the Chicago area found no evidence of a dilution effect,[48] and research in Connecticut found that C. pipiens mosquitoes preferred to take their blood meal from American robins.[45] Regardless of whether robins are the most competent or abundant hosts, "they're the most important because mosquitoes select them," notes Diuk-Wasser, who coauthored the Connecticut study.

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