CHAPTER FIVE
We stopped looking for monsters under our bed when we realized that they were inside us.
—Charles Darwin
As beautiful and deadly as predator-prey dynamics are, host-pathogen interactions take the Oscar for brilliant orchestration and level of devastation. They are literally the inspiration for Hollywood movies. In fact, Hollywood has a long history of pulling from this biological genre, because it feeds the imaginations of millions of people and pays big dividends at the box office. Think Invasion of the Body Snatchers, The Thing, Contagion, or any of the dozen or so zombie movies that have graced the big screen. The premise is simple—a pathogenic organism enters a human body and either kills its host outright or changes its behavior to do equally horrid things. Although some of these may be over the top (e.g., with body-invading organisms originating from outer space), equally disturbing creatures exist here on earth, right before our very eyes—or perhaps in them (more on this later).
While much of the Hollywood spin is fictitious, there is a kernel of truth to these movies that keeps us coming back to theaters and obsessively squirting gobs of antimicrobial soap into our palms. The threat of a mysterious organism invading our bodies—perhaps jumping from a rat, bat, bird, or cat rather than from outer space—is not just compelling, it is real. A zoonotic disease, or zoonosis, is a sickness that emerges when a pathogenic organism, such as a virus, bacterium, protozoan, or fungus, invades a human body from another animal species. Over the ages, zoonoses have been responsible for the deaths of hundreds of millions if not billions of people.
Imagine waking up with a collection of large, apple-size bulbous swellings in your groin or armpit that secrete blood and pus. Eventually, black spots start spreading all over your body, unbearable fever sets in, you start vomiting blood, and then—usually within two to seven days of the onset of symptoms—you die. The zoonotic disease responsible for these horrific symptoms, black plague, originated in China in the early to mid-1300s and then spread to Europe and the Middle East. It eventually killed about one-third of the European population—somewhere between 75 million and 200 million people. At least one more major plague pandemic would occur in the mid-nineteenth century, again starting in China, then making landfall in San Francisco and eventually going global. Today regular outbreaks of plague still occur in Africa and China, and every year in the United States there are ten to twenty cases.
The plague pathogen is a small rod-shaped bacterium called Yersinia pestis that is transmitted by a “vector,” the organism that transfers a pathogen into a host. Plague is primarily transmitted by a flea vector, whose hosts include more than 200 small rodent species such as the Great Gerbil, the Black Rat, ground squirrels, prairie dogs, chipmunks, marmots, and several other mammal hosts. Three clinical forms of plague typically emerge in humans: bubonic (the most common), pneumonic (pulmonary), and, the rarest form, septicemic, which infects the blood. In some host species, like cats, the bacteria are more likely to settle in the lungs. When this happens, cats spread the more deadly pneumonic form of the disease. People typically, but not always, contract the plague when infected fleas jump ship from a primary host and bite humans (who are known as secondary hosts, because the pathogen only invades them briefly while transitioning to its next life stage). But cat-to-human and human-to-human transmission through aerosol droplets can also lead to the deadly pneumonic plague. Finally, plague can also be contracted by eating plague-infected meat (think guinea pigs in Peru and Ecuador). Whatever the mode of transmission, after a two- to seven-day incubation period, symptoms set in and, if left untreated, death is certain and swift. If treated, approximately 50 percent of bubonic plague patients survive, but very few pneumonic or septicemic plague patients do.
It is doubtful that “John Doe,” a thirty-one-year-old man visiting Chaffee County, Colorado, had plague on his mind as he made his way into the crawl space of a house he was visiting on August 19, 1992, to catch a neighbor’s cat. Chaffee County sits almost smack-dab in the center of Colorado: it is a rural and mountainous area with a low human-population density. The cat died minutes after being brought outside. It did not occur to John Doe at the time that he should be concerned for his welfare. When interviewed days later, the owners of the cat said they had noticed abscesses, lesions, and blood-tinged sputum on the animal—all symptoms of plague infection in cats. John Doe returned to his Pima County, Arizona, home and three days later, on August 22, began feeling abdominal cramps. The following day he had a fever—his temperature climbed to 103°F—along with vomiting and diarrhea. His condition worsened, and he was admitted to a hospital on August 25. He died within twenty-four hours. Postmortem tests confirmed the causative agent of death—Yersinia pestis—the same pathogen responsible for the black plague and millions of deaths in medieval Europe. Searches around the Colorado house for infected rodents and fleas turned up a dead Colorado Chipmunk that tested positive for Y. pestis—perhaps the cat’s prey from the week before. John Doe apparently had had enough face-to-face exposure with the cat during the brief extraction from the basement for respiratory droplets to make their way into his body. The bacteria they carried killed him within a week.
Cases of plague transmitted from cats to humans are rare in the United States. From 1977 to 1998 there were twenty-three cases of cat-associated human plague in the country. At least one case occurred per year in a swath of eight western states, five of which were fatal (including John Doe’s), either because they were diagnosed too late or simply misdiagnosed. Cats transmitted plague to their owners, caregivers, and veterinarians via bites, scratches, aerosol droplets, and through the simple act of curling up on a lap and purring near the owner’s face. While most vector-borne diseases are seasonal in occurrence, plague in cats is not. These cases occurred in every month of the year but January and February and often were not associated with outbreaks of plague in nearby rodent populations. The mammal species that cats prey upon are ideal reservoirs for plague because they may remain asymptomatic throughout the year and therefore stay healthy enough to be able to transmit the pathogen if attacked or killed by a predator, which contracts the disease either through eating the infected prey or from the prey’s fleas. Plague is endemic in seventeen western U.S. states, and if you live in certain areas there (typically more rural regions with rodent populations) and you own, handle, care for, or treat an outdoor cat, you need to be vigilant for plague. In fact, wherever and whenever cats are allowed outside their owners need to be on guard for numerous disease-causing agents—many of which may not simply sicken or kill a cat but will also sicken or kill other species of wildlife—and humans.
“Cat scratch fever” can mean different things to different people depending on their frame of reference. The rock musician Ted Nugent made the phrase famous in 1977 when he released a song that metaphorically equated the disease to a man’s feverish desire for a female. More commonly (and perhaps more appropriately), cat scratch fever refers to an infection from a Bartonella bacterium that develops when an infected cat scratches or bites the human skin. In cats themselves it is usually not a serious problem, and 40 percent or so of the cats that carry it are asymptomatic. Humans, similarly, usually are not seriously harmed; a red bump forms, the lymph nodes might swell, and a mild fever may emerge. However, more serious infections can, and have, occurred, particularly among immune-compromised individuals. Although Bartonella is not as dangerous as plague, it is more common.
Cat scratches or bites can also lead to other diseases that are much more likely to be harmful. Such was the case with thirteen-year-old Grace Polhemus, of Brooklyn, New York. On October 18, 1913, while playing in her front yard, Grace bent over to pet a stray cat, and it bit her on her right wrist. It was discovered later, when brain tissue from the cat was tested, that the animal had rabies—another potentially fatal disease that can jump to humans from cats with a swipe of the paw or a quick nip of the mouth. As is often the case with rabies, the symptoms did not show up immediately in Grace. However, she died of the disease after slipping into a coma, a little over a year after being bitten.
The word rabies, taken from Latin, means “furious” or “to do violence.” A highly infectious viral disease, rabies has likely been around throughout known human history. References to rabies from as early as the fifth century BC can be found in the writings of several prominent Greek and Roman scholars and philosophers, including Democritus, Aristotle, Hippocrates, and Virgil. Up until the late 1800s, a bite from a rabid dog (the primary way humans were exposed to rabies) was a death sentence. Whether by bite or scratch, once the virus enters the body, it travels along nerve fibers, jumping neuron to neuron, slowly making its way to the brain. All mammals are susceptible to rabies, and although dogs are still sources of infection for people in Asia, Africa, and India, in North America wild animals, such as bats, foxes, skunks, and Raccoons, are thought to serve as the main reservoirs of the virus. These species can transmit the disease to domesticated species like cats, cows, and horses, which can then become vectors of the virus. When humans are exposed to the rabies virus, symptoms usually appear within one to three months of exposure. If a post-exposure prophylaxis, or treatment, is not administered, one of two forms of the disease can develop. The most common form is “furious rabies,” an early symptom of which is the fear of water—because of the difficulty swallowing—while the victim also experiences extreme thirst. For that reason rabies was also referred to as hydrophobia. Other symptoms might include hyperactivity and uncontrollable excited behavior (that is the “furious” part), extreme fever, tingling at the site of the bite, and eventually, as the virus spreads throughout the nervous system of the victim toward the brain, encephalitis (inflammation of the brain), and then death. The second type of rabies occurs in 30 percent of the cases and presents itself as a slow paralysis, usually starting at the site of the wound; patients eventually become comatose before dying. With both types, once symptoms appear death is almost certain. Fewer than ten people are known to have survived rabies infection since 1940; two of these people died within a few years of recovery from initial infection, and all but one had ongoing neurologic disorders.
Rabies is present on every continent but Antarctica. Despite the availability of highly effective pre-exposure vaccines (thanks initially to Louis Pasteur) as well as effective post-exposure prophylaxis, rabies is still responsible for more deaths per year worldwide than all other zoonotic diseases. The World Health Organization estimates that at least 60,000 people perish every year from rabies, primarily in Asia and Africa, and most of these are children under fifteen years of age. Stray dogs are still the primary reservoir and transmission mode of the disease, causing 90 percent of the exposures in Asia and Africa, and 99 percent of all human deaths. In 1946, prior to widespread vaccinations and control of stray dogs in the United States, there were 8,384 reported cases of rabid dogs and 455 cases of rabid cats. In 2010, thanks to effective and enforced policies to promote the vaccinations of owned dogs and the elimination of stray dogs, canine rabies had declined to only sixty-nine cases. The number of rabies cases in cats, however, has decreased at a less significant rate, to 303 in 2010. Since 1988 cats have been the number-one domesticated species passing rabies infections to humans. In 2013, 53 percent of all reported rabid domesticated species were cats, followed by dogs at 19 percent. The cause of this pattern seems clear—the presence of millions and millions of stray and unvaccinated free-ranging cats on the landscape, many of them sharing feeding stations with wildlife that are susceptible to rabies. Although bats, skunks, foxes, and Raccoons are the primary reservoirs of rabies in North America, cats, because of their high contact with humans, are the most important source of human exposure. The National Association of State Public Health Veterinarians does not mince words about stray cats and dogs, because of the risk of rabies and related serious health threats. The group’s policy (2011) states:
Stray dogs, cats, and ferrets should be removed from the community. Local health departments and animal control officials can enforce the removal of strays more effectively if owned animals are required to have identification and are confined or kept on leash.1
In fact, the Centers for Disease Control and Prevention and the Pennsylvania Department of Health specifically consider rabid cats to be a serious public-health concern. From 1982 to 2014 there were 1,078 laboratory-confirmed cases of rabies in outdoor domestic cats in the state of Pennsylvania (see fig. 5.1). This proliferation is likely linked to a rabies outbreak in Raccoons across the entire eastern seaboard that started in the 1950s. Outdoor cats regularly interact with Raccoons and other species when humans place food outside for wildlife and cats—especially in places like cat colonies. Such food abundance concentrates and focuses the potential for cat-wildlife interactions, providing increased opportunities for rabies transmission. Why aren’t cats in colonies immune from rabies even though they are sometimes captured, vaccinated, spayed or neutered, and then released, as part of trap-neuter-return (TNR) programs? Unfortunately, a single vaccination is not sufficient. The American Veterinary Medical Association requires revaccinations within twelve months after the initial vaccination for all cats and even recommends a recurring booster for the most effective vaccination. Catching an unowned outdoor stray or colony cat is hard to do once; doing it a second time and getting the animal revaccinated may be about as likely as a major league baseball player throwing two no-hitters in a year. Thus, most unowned cats remain unprotected against the rabies virus. (There will be much more on the shortcomings of TNR programs later; see chapter 7.) Making matters worse, people, especially children (like Grace Polhemus), are much more likely to approach a cat than they are a “wild” species like a Raccoon, and cats can shed the rabies virus for several days prior to symptoms appearing. If an interaction occurs during this period, and rabies transmission is not suspected, it will be through the onset of rabies infection only—perhaps several weeks or months later—that a rabies transmission will be known to have occurred. At that point it is likely too late.
Thankfully, the development of rabies infections in humans due to cats and other animals is extremely rare in the United States. Only a few cases appear each year. The development of highly effective post-exposure prophylaxis procedures (along with the significant reduction of stray dogs) has been critical in preventing more human deaths. Nowadays, any time a human is suspected of being exposed to a rabid animal through a bite or scratch, a post-exposure prophylaxis procedure is administered. Although no standardized reporting is done for post-exposure prophylaxis applications across the United States, the vast majority of the 38,000 post-exposure rabies treatments conducted annually are the result of people interacting with a suspected rabid cat. Each of these post-exposure prophylaxis treatments costs public-health departments and U.S. taxpayers somewhere in the neighborhood of $5,000 to $8,000, amounting to at least $190 million across the United States each year.
These diseases, which result from spillover from outdoor domestic cats, constitute a serious public-health issue. Unfortunately, there are even more-insidious disease organisms that make cats their home. These organisms are more complex in fundamental structure and have more elaborate life cycles than the bacteria and viruses that spread plague and rabies. They jump to other species and then, through a complex series of changes, both physical and chemical, get the new host to change its behavior in a way that makes it easier for the parasite to continue to reproduce and transmit. The ability of these parasites to manipulate the behaviors of their host species makes these host-parasite relationships among the most fascinating case studies in the biological world. These are the organisms that are the inspirations for zombie movies, except they are not fictional.
Toxoplasma gondii is a single-celled protozoan parasite with a worldwide distribution. It is incredible in how it maneuvers through its primary host (e.g., felines) and how it ultimately, and quite destructively, manipulates the behavior of its secondary host (e.g., other animals, including humans) to further its transmission and existence.
Toxoplasma reproduces sexually only in the intestines of domestic cats and other felines, its definitive hosts. In felines it multiplies and sexually reproduces to produce oocysts—cysts containing the Toxoplasma zygote (the two-celled body formed from the fusion of sperm and egg through sexual reproduction). These oocysts ultimately are shed in copious quantities into the environment via cat feces, a process that occurs for several weeks after a cat is initially infected. The oocysts are extremely resilient once in the environment and can persist for months to years and under all kinds of conditions, including while submerged in fresh or salt water or in frozen soil. Secondary hosts, such as mice, rats, and birds, then either intentionally or accidentally ingest the cat poop infected with Toxoplasma oocysts or pick up the oocysts from the infected environment. (Humans, of course, can also pick up the oocysts or other forms of Toxoplasma—more on this later.)
Once in the secondary host, the Toxoplasma oocysts then transform into something called a tachyzoite and multiply asexually rapidly. Tachyzoites can be as small as one-tenth the size of red blood cells when they invade healthy cells. There they divide quickly, causing tissue destruction and spreading of the Toxoplasma infection to the new host organism. Eventually the infection localizes in muscle and nerve tissue—especially in parts of the brain—in the form of cysts called bradyzoites (fig. 5.2). Then something odd begins to happen to the newly parasitized host: its normal behavior of fear toward cats turns into attraction. Specifically, the smell of cat urine—a smell that uninfected mice and rats were thought to be hardwired to fear and avoid—becomes an attractive aphrodisiac. This is exactly how the Toxoplasma parasite wants its hosts to behave, because it turns infected rodents into easy prey. Once the infected host, along with the parasites infecting its body, is eaten by a new predator (preferentially a cat or other species of feline), the parasite can begin its sexual reproductive cycle again, infecting a new host, shedding oocysts, and expanding its reach.
Does the parasite Toxoplasma really manipulate the behavior of a secondary host organism, creating an almost fatal feline attraction, for its own benefit? Researchers at Oxford University believe the answer to that question is a resounding yes. Manuel Berdoy and colleagues experimentally tested the “parasite-manipulation hypothesis” by artificially infecting lab rats with Toxoplasma to determine whether the parasite interfered with the rat’s innate reaction to predation risk by cats. The experiment consisted of examining the nocturnal exploratory behavior of twenty-three Toxoplasma-infected rats and comparing it to that of thirty-two uninfected rats. All rats appeared healthy regardless of infection status. The rats were placed in pens that had a layer of straw and a labyrinth of bricks creating a maze. Random corners of the maze were prepared with one of four treatments: the rat’s own straw bedding, fresh straw bedding treated with water, straw bedding treated with cat urine, or straw bedding treated with rabbit urine. Rats were tested individually over an entire night. The results were striking. As would be expected, healthy uninfected rats exhibited a clear aversion to the areas of the maze treated with cat urine. In contrast, and consistent with the parasite-manipulation hypothesis, rats with Toxoplasma infection exhibited an attraction to areas with cat urine. Both types of rats behaved the same way in the presence of their own smell and that of rabbits. The results were consistent with the idea that the parasite somehow subtly manipulates the brain and thus the behavior of the rat. What remained unclear was how the Toxoplasma infection, the cysts themselves, disrupted the neural circuitry of the brain and whether the attraction effect was really specific to cats—a response that would confirm the parasite-manipulation hypothesis.
The neuroscientist Robert Sapolsky, the John A. and Cynthia Fry Gunn Professor at Stanford University, decided to explore those unanswered questions. His previous research examining how stress is perceived and then translated into actual chemical signals in the body, influencing brain chemistry and action, provided a useful foundation for this exploration.
Sapolsky, along with Ajai Vyas, Patrick House, and several other collaborators, led two research projects that demonstrated that Toxoplasma infection not only eliminated a rat’s fear toward cat pheromones, it also stimulated an attraction by rats toward cats. The attraction was remarkably specific to cat urine. The group’s research confirmed that the parasite did indeed manipulate a secondary host for its own benefit through a spectacular example of host-parasite evolution. Sapolsky and his colleagues were also able to demonstrate that post infection, Toxoplasma cysts settle disproportionately near the limbic regions of the brain—the parts of the brain that control instinct, mood, defensive behavior, and sexual attraction. Toxoplasma causes rats to become almost sexually attracted to cats—an attraction that proves fatal. At least ten peer-reviewed scientific studies have now been published confirming this finding.
Why does this matter to humans? Toxoplasmosis, the disease caused by Toxoplasma gondii, is one of the most common parasitic infection in humans. In fact, it is estimated that approximately 30 to 50 percent of the world’s population and up to 22 percent of the U.S. population (more than 60 million Americans) are infected with Toxoplasma gondii—somewhat less than half of them due to direct ingestion of the Toxoplasma oocysts excreted into the environment by cats, most likely domestic cats. Many of the human infections are caused by eating infected and undercooked meat of domesticated animals that ingested the oocysts in food or water infected through cat poop. This form of toxoplasmosis lies quietly encysted in muscle and may be passed from carnivore to carnivore or omnivore (like people and pigs) and multiply in the food chain.
In some countries, human Toxoplasma infection rates are very high. Jaroslav Flegr, an evolutionary biologist at Charles University in Prague, Czech Republic, has been studying various aspects of Toxoplasma and toxoplasmosis for most of his career. He conducted a review of its prevalence in women of child-bearing age in eighty-eight countries and found that rates varied from a low of 4 percent in South Korea to highs of 84 percent, 78 percent, 63 percent, and 54 percent in Madagascar, Nigeria, Germany, and France, respectively. According to the Centers for Disease Control, humans in these various countries become infected with Toxoplasma oocysts from their environment in a variety of ways, including:
•Eating undercooked contaminated meat (especially pork, lamb, and venison) and/or accidental ingestion after handling contaminated meat and not washing hands (Toxoplasma cannot be absorbed through skin).
•Drinking water contaminated with Toxoplasma.
•Accidentally swallowing the parasite through contact with cat feces that contain Toxoplasma. This might happen by cleaning a litter box, touching anything that has come into contact with infected cat feces, or accidentally ingesting contaminated soil (e.g., from poorly washed fruits or vegetables).
•Mother-to-child congenital transmission.
•Organ transplant or blood transfusion.2
How likely is it that someone might ingest Toxoplasma oocysts, either directly or indirectly? In the United States alone 1.2 million metric tons of cat feces are defecated every year.
Despite the fact that cats are infectious and shedding oocysts for only about three weeks, oocysts are almost omnipresent. Research on the pervasiveness of Toxoplasma oocysts in California, France, Brazil, Panama, Poland, China, and Japan estimated a range of between three and 434 oocysts per square foot. Cats prefer to defecate on loose soil and often choose places like gardens and children’s sandboxes if available. As a result, such places are known to have a much higher density of Toxoplasma oocysts. Because children under three years of age are known to put their hands in their mouths every two to three minutes and can ingest a measurable amount (up to forty milligrams) of soil per day, those playing in uncovered sandboxes are at extreme risk. Most of us have encountered that small candy bar–like object while playing with our kids in the sandbox or working in the garden. Then there is our drinking water.
After rains, runoff from human-dominated environments, often covered with hardscape, moves everything from pesticides to foam peanuts to encysted protozoans, including Toxoplasma oocysts, into freshwater and marine systems. These are the very water systems that meet the needs of millions of humans—through irrigating agricultural crops (carrots, potatoes, and lettuce), maintaining livestock, and filling reservoirs that entire cities use as sources for drinking water. Toxoplasma transmitted through such means can be quite harmful. This was the case in March 1995, in Victoria, British Columbia, where an outbreak of toxoplasmosis sickened at least 100 people. The origin was traced back to the municipal water system, although it was not determined whether the source of the infection was outdoor domestic cats or wild Cougars—since individuals of both species were found around the watershed and to be actively shedding the Toxoplasma virus. This was not an isolated case. Similar outbreaks have occurred with drinking water in Panama, India, and Brazil, all in part because of the oocysts’ ability to withstand incredibly harsh conditions. Its persistence and impacts make Toxoplasma an environmental contaminant on the order of, if not worse than, DDT.
Only a single Toxoplasma oocyst needs to be consumed to result in an infection. Once the oocysts are ingested by a human, the tachyzoites divide rapidly in an acute phase of the disease. This can make a person quite sick—fever, fatigue, headaches. In people with compromised immune systems, such as late-stage HIV patients, even death can occur. It is unclear how diseases of the immune system (such as lupus, fibromyalgia, and chronic fatigue syndrome) and drugs used to suppress selected human immune function (like Cox-2 inhibitors) may affect latent Toxoplasma infections. Pregnant women and their fetuses have been known since the 1920s to be at serious risk. If infected with toxoplasmosis in the first trimester, one in ten fetuses will be aborted or become malformed—and this likely is an underreported statistic. Because of this problem, pregnant women have been warned for decades to avoid changing litter boxes and touching cat feces. Despite these warnings, congenital transfer of Toxoplasma continues to happen across the world.
In most people, a healthy immune system neutralizes active toxoplasmosis into what was thought to be a latent phase (but see below). Slowly asexually dividing bradyzoites form cysts in muscle and neural tissue (like the brain) and survive for the life of the human. The good news used to be that for the vast majority of humans living with latent-stage toxoplasmosis there were few quantifiable symptoms. Then scientists started to look a little deeper and found that bradyzoites were actually dynamic and replicating. In fact, one manifestation of toxoplasmosis infection is the development of ocular toxoplasmosis—basically cysts that settle in the eye. If the cysts burst they can cause a progressive and recurring inflammation of the retina that can result in glaucoma and eventually blindness. Regrettably, this is not the worst manifestation of toxoplasmosis infection in humans.
Thanks to recent research from Jaroslav Flegr and a handful of other pioneers (such as Manuel Berdoy, Jitender P. Dubey, Robert Sapolsky, E. Fuller Torrey, Joanne P. Webster, and Robert H. Yolken), it is becoming clearer and clearer that the latent phase of a toxoplasmosis infection is not as asymptomatic in humans as we once thought. There is now overwhelming evidence that the same behavioral changes associated with toxoplasmosis infection in rats and mice—reduced anxiety, less fearfulness, and an attraction to cat pee—are also seen in humans. Toxoplasmosis also changes human behavior—likely through changes in brain chemistry. Hundreds of studies are accumulating on the side effects of latent toxoplasmosis (detected by the presence of anti-Toxoplasma antibodies in the blood). In addition to the changes in behavior similar to those seen in rodents, individuals with latent toxoplasmosis are showing symptoms that suggest a much larger array of mental illnesses, including severe depression, bipolar disorder, obsessive-compulsive disorder, and schizophrenia. One recent study found that across twenty European countries, suicide rates in older postmenopausal women were significantly and positively associated with rates of Toxoplasma exposure. A study in Denmark enrolled a cohort of 45,788 women who gave birth to their first child between 1992 and 1995 and followed them until 2006. All the women had their levels of Toxoplasma antibodies measured. Consistent with the broader study of European women mentioned above, those infected with toxoplasmosis were two times as likely to commit suicide than the women without toxoplasmosis infection. Flegr believes that collectively toxoplasmosis, either through the acute stage of infection or through mental and neurotic illness manifested during the latent phase, has contributed to the deaths of hundreds of thousands of people, if not significantly more, over the last few decades.
Schizophrenia is a severe brain disorder in which people interpret reality abnormally, resulting in some combination of hallucinations, delusions, and extremely disordered thinking and behavior. About 1.1 percent of American adults (2.5 million individuals) live with schizophrenia; the associated costs total between $40 and $60 billion per year. Psychiatrist Fuller Torrey, the executive director of the Stanley Medical Research Institute in Chevy Chase, Maryland, has been studying schizophrenia for almost his entire career. He has written twenty books and published more than 200 papers, many of which are on the topic of schizophrenia. Torrey and neurovirologist Robert Yolken (the director of the Stanley Division of Developmental Neurovirology at Johns Hopkins University, in Baltimore) have been collaborating to understand how infectious agents, such as Toxoplasma, might be responsible for the onset of schizophrenia. In one of their papers on the topic, they conducted a review of almost fifty independent papers that examined the relationship between the presence of Toxoplasma antibodies and schizophrenia. In their meta-analysis (a statistical technique of combining the results of multiple studies into one to determine whether there is a general or overwhelming effect) they found that individuals infected with Toxoplasma were 2.7 times more likely to develop schizophrenia compared to individuals without Toxoplasma infection. Furthermore, four recent studies report that individuals with schizophrenia, compared to controls, have had more contact with cats during childhood. Today Fuller Torrey publicly states that although permanent indoor cats are relatively safe, he would not have a cat, especially a kitten, in contact with a child if the cat is going outside. He would be concerned about the risk of that child developing schizophrenia later in life. After more than twenty years of research on toxoplasmosis and various mental illnesses like schizophrenia, Torrey believes that Toxoplasma oocysts pose a significant public-health hazard. Jaroslav Flegr agrees and believes that malaria, now considered to be the most devastating protozoan killer of humans, will be “dethroned” by toxoplasmosis. As long as we continue having outdoor cats, the parasite will spread. Once humans are infected and symptomatic, most will recover. Some, however, will need to be treated with a combination of drugs, perhaps for the rest of their lives. The parasite is not likely to be eliminated, due to the locations where it encysts. It is becoming increasingly clear that toxoplasmosis is a significant zoonotic disease—perhaps one of the most significant—that impacts humans globally, and it emerges primarily from outdoor domestic cats.
Toxoplasmosis is also a significant killer of wildlife, including some of the most endangered species on the planet. When Toxoplasma oocysts contaminate our land and then pollute our fresh and marine waters through runoff, they get into food webs and eventually cause mortality in a variety of marine mammals and birds.
There are three species of monk seals on earth, all of which live in tropical marine environments. One of these species, the Caribbean Monk Seal (Monachus tropicalis), is considered extinct. Populations of another, the Mediterranean Monk Seal (Monachus monachus), are thought to hover at around 500 individuals. The third, also among the most imperiled marine mammals on the planet, is the endangered Hawaiian Monk Seal (Monachus schauinslandi; fig. 5.3). Fewer than 1,000 individuals are thought to remain, and their populations have been declining at a rate of about 10 percent a year since 1989. Distributed throughout the Northwestern Islands and the main Hawaiian Islands, Monk Seals face numerous threats, including entanglement with marine debris, food limitation, and—we now know—toxoplasmosis. Cats are in tremendous abundance all over the islands of Hawaii, and Toxoplasma has been present and circulating since at least the 1950s. When it rains in Hawaii, which it does a lot, cat feces and the Toxoplasma oocysts it contains are carried into nearshore marine waters. A minimum of eight Hawaiian Monk Seals have been found dead due to toxoplasmosis in the last ten years (two just in 2015), and this likely is a significant underestimate. The National Oceanic and Atmospheric Administration (NOAA), the branch of the U.S. federal government responsible for the management and protection of Hawaiian Monk Seals, now views free-ranging cats and the Toxoplasma oocysts they spread as a serious threat to the dwindling seals. It has become clear that cats not only kill native species directly through predation, they also do so indirectly through the shedding of Toxoplasma oocysts.
The ‘Alalā, or Hawaiian Crow (Corvus hawaiiensis), is another example, and another species endemic to Hawaii. The last two wild individuals were seen in 2002, and the species is now extinct in the wild. Thankfully, a captive breeding program had been established, and today more than 100 Hawaiian Crows are alive in captivity. The species’ initial declines were thought to have been caused by predation by rats, mongooses, and cats, as well as habitat destruction and introduced diseases like toxoplasmosis. Understanding the impacts of disease on wild birds, much as with quantifying the impacts of predators like cats, is extremely difficult to do in the field. In the 1990s, in an effort to restock populations in the wild, scientists fit twenty-seven Hawaiian Crows with radio transmitters and released them into the wild. At least five of these birds became sick with toxoplasmosis infection. One was recaptured and treated and slowly recuperated. The other four individuals were found dead in the field and were determined to have died from toxoplasmosis. Given the sensitivity of the Hawaiian Crow to toxoplasmosis, any future reintroduction efforts will need to consider the impact of free-ranging cats and Toxoplasma.
The list of species impacted by Toxoplasma infection is long, but the parasite’s predominance among marine mammals has caught scientists by surprise. The catalog of Toxoplasma casualties in marine mammals includes seals, sea lions, dolphins, Antillean Manatees, Beluga whales, and Sea Otters. And more victims are likely yet to be discovered. The ability of Toxoplasma oocysts to survive in marine environments and to move from terrestrial to marine ecosystems and up in the food chain to top-level consumers demonstrates the resiliency of these oocysts and the interconnected nature of these ecosystems.
Among marine mammals impacted by toxoplasmosis, the Sea Otter (Enhydra lutris) is one species that has been struggling to persist on the planet for a number of years and is now on the U.S. endangered species list. Sea Otters were almost wiped out in the early twentieth century, when their numbers plummeted to between 1,000 and 2,000 individuals. And while they have slowly clawed their way back in some parts of the West Coast of the United States from California to Alaska, they continue to decline in others. Hunting, oil spills, and marine pollution have been obvious culprits in Sea Otter demise. Toxoplasma infections have more recently hit the stage. A group from the University of California, Davis, and the California Fish and Game Commission trying to suss out causes of Sea Otter deaths conducted postmortem analyses of 105 dead Sea Otters collected along the California coast from 1998 to 2001. Toxoplasma infection and shark attacks were the two leading causes of mortality, and these likely were linked. Individuals with fatal shark bites were over three times more likely than those that died of other causes to have preexisting Toxoplasma infections. Given what we know about how Toxoplasma changes the behavior of rodents, we can imagine it possible that Toxoplasma-infected Sea Otters also became less fearful of their perennial predators, or at least became sick and therefore unable to escape them. Regardless, Toxoplasma gondii is a significant threat to endangered Sea Otters, Hawaiian Monk Seals, and numerous other species—including, of course, humans.
Unfortunately, there are also other deadly pathogens carried by domestic cats, including feline leukemia. This pathogen can impact both domestic and wild felines, and can be transferred from domestic animals to native species.
Feline leukemia is found in domestic cats worldwide. In the United States, 2 to 3 percent of all cats are infected with this virus, although these rates can go as high as 47.5 percent in colony cats and vary depending upon the cats’ age, sex, and condition. Once a cat is infected, feline leukemia virus can be deadly. Infected cats easily spread the virus through saliva, nasal secretions, urine, and feces. Feline leukemia virus makes cats very sick and is the major cause of cancers in domestic cats. The virus is also spread if an infected cat happens to be consumed.
One endangered feline impacted by the feline leukemia virus pathogen is the Florida Panther (Puma concolor coryi), a subspecies of the Cougar. Its populations, which once occurred throughout the southeastern United States, were decimated starting in the 1600s with massive land clearing. By the 1970s the panther had been isolated in southern Florida and was at the brink of extinction as its population size dropped to a low of twenty individuals. Today, thanks to land protection in Florida and the introduction of Cougars from Texas to reduce inbreeding, the population has grown to between 100 and 160 animals. Florida Panthers are by no means out of hot water. Other threats continue to loom, such as injuries sustained from fights with fellow panthers and collisions with cars. The consequences of small population size (as described in chapter 4) such as genetic malformations and compromised immune systems make them especially vulnerable to disease. In 2002 an outbreak of feline leukemia virus, originating from free-ranging domestic cats, reached the Sunshine State and went on to kill at least five endangered panthers through 2005. Wildlife biologists and veterinarians worked diligently to capture and inoculate as many uninfected panthers as possible with a new vaccine developed to protect them from the virus.
Two other native cats in the United States have been known to contract and die from feline leukemia virus: the Cougar subspecies of the western United States (Puma concolor couguar) and the Bobcat (Lynx rufus) throughout the country. Both of these wild felines are known to consume free-ranging cats and are likely to succumb to the disease if infected. Cat species native to other continents have also been impacted by feline leukemia virus, including the European Wildcat in Scotland, Spain, and France; the endangered Iberian Lynx in Spain; the Puma (Cougar), Ocelot, and Little Spotted Cat in Brazil; and the list goes on.
Free-ranging cats clearly pose a significant threat to a number of wild animals—birds, small mammals, reptiles—that are vulnerable to their predation. Some of the birds and animals they kill totter on the brink of extinction. However, the bacteria, viruses, and parasites cats carry and transmit—Yersinia pestis (plague), rabies virus, and Toxoplasma gondii, among others—also can drive wildlife species to extinction. Additionally, cat-transmitted pathogens have impacted millions of humans and pose one of the least understood but most critical public-health challenges of our time. Surely, some action must be taken to lessen free-ranging cats’ impact on animals and people. One solution is to remove them—once and for all—from the landscape.
1.1 A Stephens Island Wren specimen prepared by David Lyall and acquired by Walter Rothschild, from the collection of the American Museum of Natural History. (Courtesy of AMNH staff photographer Matthew Shanley)
2.1 European Wildcat (Felis silvestris silvestris), a subspecies of the Wildcat and close relative of today’s domestic cat. (Courtesy of Alex Sliwa)
2.2 Stanley Temple holding tracking equipment and one of the cats in his 1989 study in the farmlands of Wisconsin. (Courtesy of University of Wisconsin–Madison Archives)
2.3 Rachel Carson and friends on a bird walk in Glover Archibald Park, Washington, DC, September 24, 1962. (Courtesy of Shirley A. Briggs)
2.4 A Socorro Dove (Zenaida graysoni), endemic to Isla Socorro off the southern tip of Baja California and last seen in the wild in 1972. (Elizabeth Barrett)
3.1 Roger Tory Peterson, painting one of the wader plates for A Field Guide to the Birds of Britain and Europe, while staying on Hilbre Island in the Cheshire Dee, England, in October 1952. Peterson’s innovative field guides helped democratize the pastime of birding. (Courtesy of the Eric Hosking Charitable Trust)
3.2 Grumpy Cat, one of America’s favorite Internet felines, at the 2014 MTV Movie Awards. (Jaguar PS/Shutterstock)
3.3 The cover of the first edition of Peterson’s Field Guide to the Birds. (Courtesy of Houghton Mifflin)
4.1 A cat with a freshly killed Hooded Warbler (Setophaga citrina). (Shutterstock)
4.2 A cat wearing a radio collar, used in a 2004 study by Roland Kays and Amielle DeWan investigating levels of predation by owned outdoor cats. (Courtesy of Roland Kays)
5.1 Map of the distribution of laboratory‐confirmed rabid cats in Pennsylvania from 1982 to 2014. Rabies is one of many diseases that can spread from cats to people. (Courtesy of Leah Lind, PA Department of Health)
5.2 Histology slide of a protozoal cyst, or bradyzoite, of the parasite Toxoplasma gondii, which has been linked to multiple illnesses in humans, including schizophrenia and bipolar disorder. (Courtesy of D. Rotstein and NOAA)
5.3 The endangered Hawaiian Monk Seal (Monachus schauinslandi) is vulnerable to toxoplasmosis. Inshore waters can become contaminated with the bacterium’s oocysts from runoff from cat feces on land and can be potentially fatal to monk seals, Sea Otters, and other marine mammals. (Courtesy of M. Sullivan/NOAA)
6.1 The Piping Plover (Charadrius melodus) is a threatened shorebird that breeds in the northern Great Plains and along the Atlantic coast. Juveniles are especially vulnerable to predation right after hatching. (Courtesy of Frode Jacobsen)
6.2 Jim Stevenson (here holding a Western Diamondback Rattlesnake), an ornithologist based in Galveston, Texas, was at the center of a controversy concerning the killing of a free‐ranging cat in order to protect nesting Piping Plovers in 2006. (Courtesy of Jim Stevenson)
6.3 Investor turned philanthropist/activist Gareth Morgan has spearheaded a number of campaigns to revitalize New Zealand’s native species, including the Cats to Go campaign. (Courtesy of the Morgan Foundation)
7.1 Trap‐neuter‐return (TNR) advocates capture free‐ranging cats in humane traps placed near colonies. After spaying or neutering, the animals are returned to the wild, where they can continue to prey on wildlife and spread disease. (Dave Zapotosky/Toledo Blade, July 2, 2013)
7.2 A group of free‐ranging cats. Estimates place the number of unowned, free‐ranging cats in the United States at 60 to 100 million. (Shutterstock)
7.3 A PETA demonstration against fur. It is interesting to note that the animal rights organization takes a strong position against TNR, seeing adoption or euthanasia as more humane options. (S. Bukley/Shutterstock)
7.4 A spaying procedure under way. Once the cat is anesthetized, procedures take four to six minutes. The hard cost for the procedure at the Oregon Humane Society is $42.50. (Shutterstock)
7.5 While working at the San Francisco SPCA, Laura Gretch auctioned off squares of her skin to be tattooed with population control messages; the tattoo from the 2012 auction reads “Spaneuter.” Auction proceeds went to the SPCA. (Courtesy of Laura Gretch)
8.1 “Catios” allow cats to enjoy the outside while limiting exposure to other animals and automobiles. (Catio Spaces)
9.1 Michael Soule, one of the founders of the field of conservation biology, with his indoor cat, Taz. (Peter P. Marra)
9.2 Two fabricated Stephens Island Wrens (Xenicus lyalli) in a setting reminiscent of their historical habitat on display in Te Papa Tongarewa (National Museum of New Zealand). (Courtesy of the National Museum of New Zealand, Te Papa Tongarewa)