Spillover: Animal Infections and the Next Human Pandemic (31 page)

And so that was tried. In one early effort, on a small island off Cape Cod, state wildlife biologists shot 70 percent of the deer; then researchers assessed the effect on tick populations by counting tiny, immature ticks on one kind of mouse. Result: The abundance of ticks on the mice was at least as high as before deer eradication. In years since, heavy deer-hunting has been encouraged in some areas of Maine, Massachusetts, Connecticut, and New Jersey for the sake of drawing down deer populations, while researchers again monitored the effects, if any, on populations of ticks. The town of Dover, Massachusetts, for instance, recently announced its first deer hunt on open town land, reflecting recommendations from the local board of health and the Lyme Disease Committee. Nineteen deer (sixteen does and three bucks) were killed, after which a Dover newspaper explained confidently: “
The higher the number of deer in an area
, the higher the chances are of spreading Lyme disease to humans.”

Well, actually, no. That simple formula is as false as the notion that swamp vapors bring malaria.

The premise behind such civic efforts is that the landscapes in question contain “too many” deer and that their overabundance accounts for the emergence of Lyme disease since 1975. And it’s true enough that there are
lots
of deer out there. Populations in the northeastern United States have rebounded robustly (because of forest regrowth, absence of big predators, lessened hunting by meat-hungry humans, and other factors) since the hard times of the eighteenth and nineteenth centuries. There might be more deer in Connecticut today than at the time of the Pequot War in 1637. But that abundance of whitetails, as Ostfeld’s work showed, is probably irrelevant to the chances you’ll catch Lyme disease during a stroll in, say, Cockaponset State Forest. Why?

“
Any infectious disease is inherently an ecological system
,” Ostfeld wrote. And ecology is complicated.

51

R
ick Ostfeld, seated in his office at the Cary Institute of Ecosystem Studies, in Millbrook, New York, his walls and door decorated with tick humor, told me that he’s a “heretic” on the subject of deer and Lyme disease. But he’s a heretic with data, not one who listens to private voices of revelation.

Ostfeld is a fit, cheerful, fiftyish man with short brown hair and ovoid glasses. His primary research interest is small mammals. He studies the ways they interact, the factors affecting their distribution and abundance, the effects of their presence or absence, the things they carry. Since the early 1990s, he and his group at Cary have live-trapped tens of thousands of small mammals in the forest patches of Millbrook and neighboring areas—mainly mice, chipmunks, squirrels, and shrews, but also creatures as large as possums, skunks, and raccoons. Initially his research had nothing to do with Lyme; he was tracing population cycles of a native rodent, the white-footed mouse. Many kinds of small mammal tend to show such population cycles, passing from relative scarcity one year to abundance the next, even greater abundance the year after, and then crashing back to scarcity, as though governed by some mysterious rhythm. Many mammal ecologists have studied such cycles, trying to determine their causes. What drives the boom and the bust?

Ostfeld was more curious about the consequences. When animal A becomes inordinately plentiful, how might that affect the populations of animals B, C, and D? Specifically, he wondered whether high population levels of white-footed mice might control outbreaks of a certain pestiferous moth by eating up most of the caterpillars. As he trapped his animals, examined them, and marked them with ear tags before release back into the understory, he noticed that their ears were covered with tiny dark bodies, as small as the dots of a colon: baby ticks. The mice were infested. They were supplying blood meals to the immature stages of
Ixodes scapularis
, known to Ostfeld as
the
blacklegged (not “deer”) tick. “
Thus began my interest in Lyme disease ecology
,” he wrote in the preface of his book.

Over those twenty years, mammal by mammal, tick by tick, Ostfeld and his team collected an enormous body of information, and the work continues. They use Sherman live traps (from the H. B. Sherman company, of Tallahassee, a venerable supplier) baited with oats and set out on the forest floor. They release most of the captured animals alive, after a brief examination to check body condition and remove ticks. Small mammal biologists like him, for whom trap-and-release protocols are the daily routine of data gathering, tend to become highly adept—gentle but efficient—at handling live rodents. Ostfeld’s group has found that, in about one minute of close scrutiny, they can detect 90 percent of the ticks on a mouse. (They measured their own field-exam thoroughness by taking some mice into captivity after the one-minute check-over, holding them captive, and waiting for all ticks to fall off into a pan of water beneath the cage. Then they sorted the ticks from the mouse shit and other detritus—“
a messy and challenging task
,” Ostfeld testified—and counted this fuller total for comparison with what had been seen in the field.) For chipmunks, the method of quick visual inspection worked almost as well. On other small mammals, including squirrels and shrews, the tick burdens were higher and harder to count, but Ostfeld’s group could still make well-informed estimates.

Larval ticks are minuscule and even a tiny masked shrew, weighing only five grams (about the same as two dimes), carried on average fifty-five ticks, the researchers found. That’s a mighty burden of infestation for such a small, delicate creature. The short-tailed shrew, a larger animal, averaged sixty-three ticks per animal. Given Ostfeld’s estimate (also derived from trapping data) of about ten short-tailed shrews resident in an acre of woodland around Millbrook, it begins to add up to quite a few ticks, whole forests a-crawl with sanguineous dots, a disquieting prospect, even if the blacklegged tick
never fed on anything but the blood of shrews.

But it does. Its life cycle is complex. Like an insect, the blacklegged tick undergoes metamorphosis, passing through two immature stages (larva and nymph) on the way to adulthood. At each of those stages, it needs a single blood meal from a vertebrate host to nourish its transmogrification; an adult tick needs another blood meal to supply energy and protein for reproduction. In most cases the vertebrate host is a mammal, though it might also be a lizard, or a ground-nesting bird such as the veery, exposing itself to larval ticks on the forest floor. The blacklegged tick is such a generalist, in fact, that its menu of known hosts includes more than a hundred North American vertebrates, ranging from robins to cows, from squirrels to dogs, from skinks to skunks, from possums to people. “These ticks are unbelievably catholic in their tastes,” Ostfeld told me.

An adult female tick spends her winter with a bellyful of blood and then in spring lays her eggs, which hatch into larvae by midsummer. Whether as immatures or as adults, ticks can’t travel very quickly or very far. They don’t fly. They’re not so acrobatic as fleas or springtails. They lumber around like tiny tortoises. But they seem to be “
exquisitely sensitive
” to chemical and physical signals, according to Ostfeld, and thereby “able to orient toward safe locations for overwintering and toward hosts emitting carbon dioxide and infrared radiation.” They smell out their food. They may not be agile, but they’re opportunistic, alert, and ready.

The complete life cycle takes two years and entails three distinct episodes of parasitic drinking, each of which can involve a different kind of vertebrate host. Acarologists (tick biologists) have a wonderfully high-flown term for the behavior by which a tick seeks its next attachment, climbing to the top of a grass stem or out to the edge of a leaf, front legs extended, sniffing the signals, positioned to grab a new host;
the word is
“questing.” The smaller the life stage, the more likely that questing occurs very low to the ground. One consequence of this, reflected in the data of Ostfeld and his colleagues, is that those two kinds of shrew supply about 30 percent of all the blood meals taken by larval ticks in the study area. White-footed mice are second in importance as blood hosts for the larval stage.

White-tailed deer seem to play a much different role. They are important mainly to adult ticks—not just for their blood, but also for providing a venue where male blacklegged ticks can meet females. A whitetail in the woods of Connecticut, during November, is like a teeming singles’ bar in lower Manhattan on Friday night, crowded with lubricious seekers. One poor doe might be carrying a thousand mature blacklegged ticks. Mating occurs, somewhat gracelessly, when a male tick, prowling across the skin of the deer, encounters a preoccupied female—she is tapped in, drinking, immobile. Don’t look for romance in arachnoid sex. Once the female has had her drink, and the male has had his congress, they drop off the deer, making way for others. Given such turnover, during a four-week season of tick procreation, a single whitetail can supply blood for the production of 2 million fertilized tick eggs. If half of those hatch, it’s a million larvae from one deer.

Such data and calculations helped make Rick Ostfeld a heretic on the significance of deer in the Lyme disease system. The prevailing assumption was that more deer yield more ticks and therefore more risk of disease. “But it looks like all you need is a
few
deer to support a very abundant tick population,” he told me. The more important risk factors, in an area like coastal Connecticut, might be local abundance of white-footed mice and shrews. Who knew?

But hold on. We’re dealing with ecology, therefore complexity, and two additional factors must be considered. One is an unchanging fact and one is a variable. The unchanging fact is that
Borrelia
burgdorferi
infection doesn’t pass vertically between blacklegged ticks. In plainer language: It is not inherited. Of those million baby ticks, all derived from the female ticks that fed on a single deer, none will be carrying
B. burgdorferi
when they hatch—not even if every mother tick was infected and the deer was too. The youngsters will come into the world clean and healthy. Each generation of ticks must be infected anew. Generally what seems to happen is that a larval tick acquires the spirochete by taking its blood meal from an infected host—a mouse, a shrew, a whatever. It molts to become a nymph and then, if it gets its next meal from an uninfected host, the nymph passes the infection to that animal, by drooling spirochetes into the wound along with its anticoagulant saliva. “If mammals didn’t make ticks sick,” Ostfeld said, “ticks wouldn’t make mammals sick later on.” Such reciprocal infectivity helps keep the prevalence of
B. burgdorferi
high in both tick populations and hosts.

Related to the unchanging fact of noninheritability is a variable that
Ostfeld and others call
“reservoir competence.” This is the measure of likelihood that a given host animal, if it’s already infected, will transmit the infection to a feeding tick. Reservoir competence varies from species to species, most likely depending on differences in the strength of immune response against the pathogen. If the immune response is weak and the blood teems with spirochetes, that species will serve as a highly “competent” reservoir of
B. burgdorferi
, transmitting infection to most ticks that bite it. If the immune response is strong and effective, damping down the level of blood-borne spirochetes, that species will be a relatively less competent reservoir. Studies by Ostfeld’s group, involving captive animals and the ticks feeding on them, showed white-footed mice to be the most competent of reservoirs for the Lyme disease spirochete. Chipmunks were a distant second in reservoir competence, with shrews close behind them.

Further complication: Besides being very competent as reservoirs, white-footed mice are also inefficient groomers, poor at clearing off the ticks, which target especially their faces and ears, so that a high percentage of their ticks survive into later stages. Shrews are also inefficient self-groomers, unfortunately for them, and therefore mice and shrews contribute disproportionally to the feeding, infecting, survival, and successful metamorphosis of larval ticks. By this standard, chipmunks were third in overall importance.

What matters perhaps less than their relative rankings is the more general point that these four little mammals together weigh so heavily in the system. Summary statistics compiled by Ostfeld and his gang indicate that up to 90 percent of the infected nymphal ticks “questing” for their next hosts, in a typical forest patch near Millbrook, New York, had taken their larval blood meal from (and therefore been infected by) either a white-footed mouse, a chipmunk, a short-tailed shrew, or a masked shrew. Those four hadn’t fed 90 percent of all blacklegged nymphs but, because of the differences in reservoir competence and grooming efficiency, they had fed 90 percent of those that became infected and dangerous to people. Should I repeat that? Four kinds of small mammal fueled nine-tenths of the disease-bearing ticks.

So forget about deer abundance. White-tailed deer are involved in the Lyme disease system, yes, but involved like a trace element, a catalyst. Their presence is important but their numerousness is not. The littler mammals are far more critical in determining the scale of disease risk to people. Adventitious years of big acorn crops, yielding population explosions of mice and chipmunks, are more likely to influence the number of Lyme disease cases among Connecticut children than anything that deer hunters may do. Beyond helping the blacklegged tick
(infected or uninfected) to survive, white-tailed deer are almost irrelevant to Lyme disease epidemiology. They don’t magnify the prevalence of infection in the forest. They don’t pass the spirochete to humans or to newly hatched ticks. They’re dead-end hosts, Ostfeld told me.

Then again, he said, “We also happen to be dead-end hosts, in that, once we’re infected, the infection goes nowhere. It stays in our body. It doesn’t go back into ticks. So we’re an incompetent reservoir.” Mice and shrews make the ticks sick; the ticks make us sick; and we don’t make anybody sick. The
Borrelia burgdorferi
spirochete, if a person catches it, stops there. It doesn’t travel on a sneeze or a handshake. It doesn’t move downwind. It’s not an STD. This is interesting ecologically but probably cold consolation to anyone suffering from Lyme disease.