Ticks, Squirrels, Lizards, and Spirochetes

By Joe Eaton
Tuesday June 21, 2011 - 03:45:00 PM
Western gray squirrel: reservoir species for the Lyme pathogen.
Mary Cummins
Western gray squirrel: reservoir species for the Lyme pathogen.
Southern alligator lizard: major player in the ecology of Lyme disease.
Pierre Fidenci
Southern alligator lizard: major player in the ecology of Lyme disease.

Science writers are always in pursuit of a moving target. Unless you stick to a specialized beat, you often find yourself revisiting a subject you reported on earlier and finding that quite a bit has happened in the interim.

That’s certainly true of the research on the natural setting of Lyme disease, much of which has come out of the lab of UC-Berkeley medical entomologist Robert S. Lane. The last time I wrote about the disease was eleven years ago, shortly after May Kuo, then one of Lane’s graduate students, had identified the substance in the blood of western fence lizards and southern alligator lizards that kills the Lyme disease spirochete Borrelia burgdorferi. An infected western black-legged tick (Ixodes pacificus) can no longer transmit the disease after a blood meal from one of either of these lizard species. The substance, for the record, is a set of proteins called the alternative complement pathway. It’s a good thing both lizards are abundant within the tick’s California range. Other lizards have no apparent effect on the pathogen. 

(Gratuitous factoid about lizard blood, which is how I stumbled back into the Lyme story in the first place: New Guinea skinks of the genus Prehinsohima have green blood. Seriously. Unlike in Vulcans, the coloration is the result of a high concentration of the bile pigment biliverdin. What might green blood be good for? Field studies suggest that the biliverdin protects the lizards against the malaria organism Plasmodium and other blood parasites. It may also make them taste bad to predators.) 

There have been some interesting developments since then. David Perlman probably knows all about them, but I didn’t until I started working my way through the science journals. 

Back in 2000, Lane and his associates were still looking for another piece in the Lyme puzzle. Many infectious diseases of humans persist in a reservoir comprised of other vertebrate species. The pathogen doesn’t kill the host, and retains the potential to spread to humans that have contact with the reservoir organism. The historic reservoir for the bubonic plague was a Central Asian marmot; in North America, prairie dogs and other ground squirrels have become plague reservoir species. 

Identifying the Lyme disease reservoir(s) in California was an obvious priority. Earlier work had pointed toward dusky-footed woodrats, California kangaroo rats, and deer mice as reservoir species in chaparral habitats. But these small rodents were scarce in wooded areas where the disease was endemic. What was the woodland reservoir? 

One line of research looked for candidate hosts for the black-legged tick. With Lars Eisen and Rebecca Eisen, Lane sampled oak-woodland habitat near Hopland in Mendocino County, home of the Mendocino Brewery, for birds, lizards, and small mammals. Unsurprisingly, they found a lot of larval ticks on the fence and alligator lizards, of which 86 to 89 percent were infested with an average of 18 ticks per lizard. For the nymph stage of I.pacificus, fence lizards and western gray squirrels carried similar tick loads. The squirrels were far ahead of other rodents like woodrats and deer mice. Bird infestation was generally low: Anna’s hummingbirds, bushtits, and lesser goldfinches were tick-free, while dark-eyed juncos had an average of 1.18 larval ticks. 

Lane and the Eisens went on to test additional Hopland western gray squirrels for the Lyme spirochete. Eight of ten squirrels proved to be positive for B. burgdorferi. Almost half of the larval black-legged ticks that fed on the squirrels’ blood became infected with the spirochete. The squirrel, then, met the criteria for a reservoir species: it could keep the pathogen alive from year to year and infect or reinfect its vector. The authors noted that western grays spend considerable time foraging on the ground, where the ticks can get at them, and that young squirrels leave their arboreal nests in mid-April when the number of host-seeking tick larvae and nymphs approaches or reaches its annual peak. 

Broadening the search, another team trapped a total of 222 western gray squirrels at China Camp State Park in Marin County, Annandel State Park in Sonoma County, and, once again, Hopland, as well as other areas from Humboldt County to Los Angeles. The prevalence of B. burgdorferi infection was highest in the northwestern counties. The researchers also found a strong relationship between western gray squirrel infection prevalence and the incidence rates of human cases of Lyme disease on a county basis. Squirrels of other species found their way into the traps, but only two individuals tested positive: an eastern fox squirrel from Alameda County (one out of 64) and an eastern gray squirrel from Santa Cruz County (one out of 14.) That’s one less thing to worry about for those of us who are plagued with the exotic fox squirrels. 

The most recent installment of the squirrel story that I’ve been able to locate is an article by Lane and Daniel Salkeld, published last year in Evolution. They developed a mathematical model incorporating lizard and squirrel abundance, larval tick loads, and infection prevalence, and reported that its predictions of Lyme disease risk closely matched real-life data. 

This body of research should not, of course, be interpreted as a call to go out and eradicate western gray squirrels, or try to increase lizard populations (however you might do that.) The tick-lizard-squirrel dynamic appears to be highly complex. “The roles of hosts in supporting both pathogen and vector must be well understood before control efforts attempting to manipulate the host community ecology are undertaken,” Lane and Salkeld conclude. Amen to that. Aldo Leopold, once again: “To keep every cog and wheel is the first precaution of intelligent tinkering.”