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The Ecology of Lyme-Disease Risk

Complex interactions between seemingly unconnected phenomena determine risk of exposure to this expanding disease

Richard Ostfeld

The Acorn Connections

Since the number of infected nymphs emerging in any given season has some bearing on the number of people potentially exposed to the bacterium, it is important to determine how many infected nymphs emerge within a given habitat type in any given year. Recent research in my laboratory reveals that one of the most powerful predictors of nymph numbers is the number of acorns in a particular area. The episodic or periodic production of bumper crops of acorns, a phenomenon known as "masting" behavior by oak trees, sets off an ecological chain reaction that influences distribution and infection rates of ticks, and hence risk of Lyme disease. White-tailed deer consume woody browse during much of the year, but during mast years, when acorns are abundant, deer favor acorns during autumn and winter. William McShea at the National Zoological Park in Front Royal, Virginia, and coworkers placed radio transmitting collars on deer and monitored their movements and thus their use of different habitat types. These studies demonstrated that deer concentrate their activities in oak-dominated forest stands during the autumn of mast years, but they avoid oak stands in nonmast years, probably because the quality of woody browse is better in other forest types.

Figure 7. Population densities of larval ticks . . .Click to Enlarge ImageFigure 8. Densities of white-footed mice . . .Click to Enlarge Image

At my laboratory's study sites in southeastern New York State, mast production was heavy in 1991 and 1994, with few acorns produced in 1992, 1993, 1995 and 1996. My colleagues, Clive Jones of the Institute of Ecosystem Studies and Jerry Wolff at Oregon State University, and I therefore expected that in the autumns of 1991 and 1994, deer would concentrate their activities in oak-dominated patches, that they would import their burdens of adult ticks into oak stands, and that oak forests would be the primary sites where the ticks would mate and lay their eggs. We predicted that oak stands would be infested with newly hatched larval ticks in the summers of 1992 and 1995—that is, the summers following heavy mast production. In contrast, for the summers following mast failure, we predicted that larval ticks would be most abundant in other habitat types, since we also predicted that deer would avoid oak forests in nonmast autumns.

To test this prediction, we made estimates of relative tick populations in five different habitats (two forest types and three types of open fields, with three replicate sites for each type) based on samples we culled from each. To sample tick abundance, we used a standard technique that involves dragging a one-square-meter piece of white corduroy cloth along premeasured lines 100 meters long and stopping every 15 meters to count the ticks that attach to the cloth.

We found that the location of peak abundance of larval ticks shifts dramatically from year to year, coinciding with the presence or absence of acorns in oak stands the prior fall. Oak forests were the sites of larval-tick outbreaks in the summers following acorn years, whereas maple forests were most heavily infested in summers following acorn failure. Subsequently, together with Clive Jones, Jerry Wolff and several technicians, I added almost 1 million acorns to three 2.25-hectare forest plots during the autumn of a year of very poor natural-acorn production. As a control, we monitored three matched plots to which no acorns were added. The following summer we observed that densities of larval ticks were approximately 10 times higher in acorn-supplemented plots than in control plots. This result supports our proposed link between acorn availability, space use by white-tailed deer and location of larval-tick outbreaks.

Figure 9. Factors within oak-forest ecosystems . . .Click to Enlarge Image

Deer are not the only wildlife species that rely strongly on acorns as a food resource. Long-term studies of population dynamics of white-footed mice, conducted by Jerry Wolff in Virginia, by Steven Vessey at Bowling Green State University in Ohio, by Joseph Merritt at the Powdermill Biological Station in Pennsylvania, and by ourselves in New York, reveal that the abundance of mice in a particular area is closely tied to acorn production. In the fall of a mast year, mice both consume and store acorns in large numbers. Consequently, during the winters following mast production, mice tend to experience higher-than-normal survival rates. Winter breeding by white-footed mice almost never takes place when acorns are unavailable. In contrast, mice breed rampantly during postmast winters and begin the normal spring-breeding season at high density and in good physiological condition. Mouse populations then reach peak density by the middle of the summer following a mast year.

By influencing the use of space by deer and the population dynamics of mice, acorn production is tied to peaks in abundance of both larval ticks and mice, the most reservoir-competent host, in oak forests during the summer following a mast year. Currently, my colleagues and I are testing the prediction that, because of greater densities of mice in the postmast year, larval ticks have a higher probability of feeding on this reservoir species and consequently of acquiring the Lyme-disease-causing bacterium. If this is true, we expect bacterial-infection rates of nymphal ticks to be highest two years following heavy acorn production, an expectation that is currently being tested by dissecting ticks and examining their tissues for the presence of B. burgdorferi. Because the abundance of infected nymphal ticks is the primary ecological risk factor in the Lyme-disease epidemic, it is clear that masting behavior by oaks may have crucial consequences for Lyme-disease epidemiology.

Based on heavy acorn production in 1991 and 1994, we predicted that 1993 and 1996 would be years of particularly high incidence of Lyme disease. Statistics from the county health departments in southeastern New York state indicate that, although 1993 was an average year for Lyme disease, 1996 saw an unusually high number of cases. A robust test of our model’s accuracy will require at least several more years of monitoring mast production and Lyme disease cases. In addition, it will be important to determine over how large an area oak trees are synchronized in their mast production, because it is only within these areas that we expect Lyme disease risk to be correlated with acorn production two years earlier.

Based on heavy acorn production in 1991 and 1994, we predicted that 1993 and 1996 would be years of particularly high incidence of Lyme disease. Statistics from the county health departments in southeastern New York state indicate that, although 1993 was an average year for Lyme disease, 1996 saw an unusually high number of cases. A robust test of our model’s accuracy will require at least several more years of monitoring mast production and Lyme disease cases. In addition, it will be important to determine over how large an area oak trees are synchronized in their mast production, because it is only within these areas that we expect Lyme disease risk to be correlated with acorn production two years earlier.

The studies summarized above are ongoing, but they provide hope that various forest and field types can be risk-rated for Lyme disease well in advance. Ultimately, we expect that, just as fire risk is posted at many national and state parks and forests each season, further studies of links between acorns, deer, mice, ticks and spirochetes will allow us to warn the public which areas to avoid and when to avoid them.





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