Spillover

by David Quammen

  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.

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  Ostfeld is sensitive to the human toll, not just to the wondrous intricacy of Borrelia burgdorferi dynamics in American forests. He showed me some figures from Dutchess County, New York, which includes Millbrook and the Cary Institute, between 1986 and 2005. The twenty-year trend of human infections was steeply upward, with especially high peaks in 1996 and 2002. People were suffering. In 1996 there were 1,838 reported cases of Lyme disease. After that came a sizable decline until, in 2002, again almost two thousand new cases were reported.

  Still, it’s best understood as an ecological phenomenon, not just a medical problem. “Lyme disease in humans exists because we are sort of unwitting victims of a wildlife-tick interaction,” Ostfeld said. “We’re interlopers into t
his system where ticks and these hosts—the reservoir hosts—pass bacterial infections back and forth.” One way of construing those peaks in 1996 and 2002, he explained, is that they reflect autumns of bounteous production in the local forests. White-footed mice love acorns and, because the mice reproduce quickly and mature quickly, responding to food abundance with bursts of heightened fecundity, big masting events are often followed (after a two-year lag) by big increases in the mouse population. One pair of mice, given circumstances of plentiful food, could produce a net gain of fifty to seventy-five mice within a year. More acorns, more mice, more infected ticks, more Lyme.

  Dutchess County is a halcyon Yankee getaway just east of the Catskills and only two hours from Manhattan via the Taconic State Parkway. It’s a landscape of rolling hills, stone fences, small towns, old roadhouses, little gullies and streams carrying rain to the Hudson River, golf courses, and suburban neighborhoods, including some graceful homes with sizable yards shaded by hardwood trees and bordered by hedges or feral brush. The residential areas, even the commercial districts and malls, are well garnished with greenery. Scattered between and around the zones of concentrated human presence are parks, woodlots, and forest patches, dominated not by people but by oak and maple. The understory of those patches is rife with mosses, leaf litter, barberry, chickweed, acorn scraps, poison ivy, wild mushrooms, rotting logs, soggy swales, and the newts, frogs, salamanders, crickets, pill bugs, earthworms, spiders, and garter snakes that thrive in such places. Ticks too, of course—manymanymany ticks. During the year before my visit, Dutchess County health authorities had recorded another 1,244 cases of Lyme disease within a resident population of less than three hundred thousand people. It was enough to make you think twice about a stroll through the woods.

  Ostfeld and his team can’t afford to be squeamish, though, because those forest patches are where they gather their data. I had tagged along earlier that day, walking trap lines with him and some of his young colleagues. One of them was Jesse Brunner, a postdoc from Helena, Montana, bearded and balding, who was engaged in a multiyear study exploring the correlation, if any, between Lyme prevalence and species diversity on forest patches of various sizes. Another teammate was Shannon Duerr, a tech assistant employed in Ostfeld’s lab, presently suffering a case of Lyme disease herself and under treatment with amoxicillin. Ostfeld, I noticed, wore his jeans tucked into his socks as we moved through the forest, and he worked in latex gloves while handling a captured animal. Jesse Brunner showed me his own technique with a white-footed mouse, and then handed the creature to me.

  I held the mouse, as instructed, with a gentle pinch of the skin over its shoulders. Its eyes were dark and huge, protrusive with fear, gleaming like steel BBs. Its ears were large and velvety. Its fur was a soft brownish gray. Attached to one ear I could see several dark dots, each no bigger than a period. Those were larval ticks, Brunner explained; they had recently come aboard and scarcely begun to drink. In the other ear was a larger black lump, big as a pinhead. That larva had been attached longer and was now engorged with blood. At this time of the season, Brunner told me, the mouse was probably already infected with B. burgdorferi from the bite of a nymphal tick. The engorged larva had probably just become infected, in turn, from the mouse. So I was holding, most likely, two infected carriers. As I listened raptly to Brunner, the mouse sensed my lapse of attention, sprang free of my grip, hit the ground running, and disappeared in the undergrowth. And so the cycle continued.

  That afternoon, during our chat in his office, I asked Ostfeld a practical question: Say you’re a parent with young children, living here in your Millbrook dream house on three acres of beautiful lawn and shrubbery—what do you want for protection against Lyme disease? There might be a whole range of desperate options. Pesticide spraying by the county? Deer eradication by the state? Thousands of mousetraps (not Shermans but the lethal kind), deployed in the forest and baited with cheese, snapping away like brushfire? Do you pave your yard and ring it with an oil-filled moat? Do you put flea-and-tick collars on your kids’ ankles before they go out to play?

  No, none of those. “I would feel a lot more comfortable,” Ostfeld answered, “if I knew that the landscape would support healthy populations of owls, foxes, hawks, weasels, squirrels of various kinds—the components of the community that could regulate mouse populations.” In other words, biological diversity.

  This was his offhand way of expressing the most notable conclusion that has emerged from twenty years of research: Risk of Lyme disease seems to go up as the roster of native animals, in a given area, goes down. Why? Probably because of the differences in reservoir competence between mice and shrews (both with high competence) and almost all other vertebrate hosts (low competence) that may share habitat with them. The effect of the most competent reservoirs is diluted by the presence, when there is such presence, of less-competent alternatives. In forest patches containing a full cast of ecological players—medium-sized predators such as hawks, owls, foxes, weasels, and possums, as well as smallish competitors such as squirrels and chipmunks—the populations of white-footed mice and shrews are relatively small, held in check by predation and competition. The average reservoir competence is therefore low. In forest patches with little diversity, on the other hand, white-footed mice and shrews are almost certainly there, flourishing inordinately. And where they flourish, transmitting infection efficiently to the ticks that bite them, Borrelia burgdorferi flourishes also.

  This insight had led Ostfeld to another interesting question, one with direct implications for public health. Which forest patches contain less species diversity than others? In practical terms: Which woodlots and green zones and parks harbor the greatest risk of exposure to Lyme disease?

  Bear in mind that any patch of forest, surrounded by pavement and buildings and other forms of human impact, is to some degree an ecological island. Its community of land animals is insularized because, when individuals try to leave or to enter, they get squashed. (Birds are a special case, though they tend to conform to the same pattern.) Be aware too that big islands generally support more diversity than small islands do. Madagascar is more richly diverse than Fiji, which in turn is more richly diverse than Pohnpei. Why? The simple answer is that greater land area and greater habitat diversity allow the survival of more kinds of creatures. (The complicated details behind that simple answer are addressed by a field of science called island biogeography, familiar to Rick Ostfeld because it so heavily influenced ecological thinking during the 1970s and 1980s, and familiar to me because I wrote a book about it in the 1990s.) Apply that principle to Dutchess County, New York, and it yields a prediction that small forest patches, postage-stamp woodlands, contain fewer kinds of animal than larger forest tracts. That’s what Rick Ostfeld did—applied the prediction of area-related diversity as a rough hypothesis and then studied real sites to test it. By the time of my visit to Millbrook, he could say that the pattern did seem to hold true, while Jesse Brunner’s postdoctoral work probed further into the same topic.

  Then time passed. Five years after I spoke with him, Rick Ostfeld could state the matter more confidently based on two decades’ worth of continuous investigation. It became an important theme in his Lyme Disease book. With his increasing confidence in the general principles has come increasing appreciation for the various ways those principles play out in differing circumstances. All his conclusions are now carefully modified with conditionals. But the basic findings are clear.

  A tiny patch of woodland in a place such as Dutchess County is likely to harbor only a few kinds of mammal, one of which is the white-footed mouse. The mouse is a good colonizer, a good survivor, a fecund breeder, an opportunist; it is there to stay. Restrained by few predators and few competitors, its population fluctuates around a relatively high average level and, in summers following a big acorn crop, goes much higher still. A plague of mice will infest the little woodland, like rats on the road out of Hamelin. There will also be plenty of ticks. The ticks dr
ink heartily of mouse blood and have a high rate of survival, because white-footed mice (unlike possums, catbirds, or even chipmunks) are not very good at grooming themselves clear of larvae. And because the mouse is such a competent reservoir of Borrelia burgdorferi—so efficient at harboring and transmitting it—most ticks carry the infection.

  In a larger area of forest, with a more richly diverse community of animals and plants, the dynamics are different. Facing a dozen or more kinds of predators and competitors, the white-footed mouse is less numerous; the other mammals are less competent as hosts for the spirochete and less tolerant of thirsty tick larvae; the net effect is fewer infected ticks.

  Although it’s an intricate system, as Ostfeld warned in his title, certain points about Lyme disease emerge plainly. “We know that walking into a small woodlot,” he wrote, “is riskier than walking into a nearby large, extensive forest. We know that hiking in the oak woods two summers after a big acorn year is much riskier than hiking in those same woods after an acorn failure. We know that forests that house many kinds of mammals and birds are safer than those that support fewer kinds. We know that the more opossums and squirrels there are in the woods, the lower the risk of Lyme disease, and we suspect that the same is true of owls, hawks, and weasels.” As for white-tailed deer: They’re involved, yes, but far from paramount, so don’t believe everything you’ve heard.

  Some people take “All life is connected” to be the central truth of ecology, Ostfeld added. It’s not. It’s just a vague truism. The real point of the science is understanding which creatures are more intimately connected than others, and how, and to what result when change or disturbance occurs.

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  One of the signal lessons of Lyme disease, as Rick Ostfeld and his colleagues have shown, is that a zoonosis may spill over more readily within a disrupted, fragmented ecosystem than within an intact, diverse ecosystem. Another lesson, though, has little to do with Ostfeld’s work and can’t be addressed at the scale of Sherman traps baited with oats. This one derives from a more basic fact—the fact that Borrelia burgdorferi is a bacterium.