The Fever

by Sonia Shah

  4. MALARIAL ECOLOGIES

  Malaria is not a disease of the environment in the way that, say, asthma is or certain kinds of cancer are. And yet its transmission depends upon an exacting set of environmental conditions. The protozoan parasite, despite all its sophisticated wiles and cunning, is more like a seed than a self-sufficient predator. Like a pip on the wind, it must alight in a fertile bed, be enveloped in the proper amount of moisture, and be bathed in the correct level of sunlight. The right mosquito must bite at the right time and with the correct frequency. If a local mosquito bites the wrong host, or if the insect’s body becomes too cool or too warm, or if it dies or fails to bite before the parasite has time to develop inside its body, Plasmodium, one of the world’s most deadly pathogens, might as well be an inert gas.

  The circumstances that decide malaria’s fate are contingent upon other circumstances equally beyond the parasite’s control. The biting behavior of the mosquito, for example, depends partly on the species and partly on the variable availability of blood-filled hosts. Some species, such as Anopheles gambiae, are deeply connected to human hosts. Others are not so picky and will happily feed on the blood of cows or horses, if these happen to be available. The longevity of a mosquito, too, depends on multiple factors, such as the mosquito’s habits and where she takes her blood meal. The female must rest soon after a feast, to excrete the excess liquid from her body. Will this siesta occur nearby, in a safe, snug place, or will it require some dodgy flight, in which she crosses paths with a swatting hand or swooping predators? What kind of weather will the blood-engorged insect encounter? Arid conditions, for example, can be deadly.

  Of all the micro-geographic and climatic forces affecting malaria, the single most important factor is the species of the local population of mosquito. Of the planet’s 430 different species of Anopheles mosquito, some 70 species transmit malaria. Each specializes in a specific geographic and climactic zone, be it the temperate Americas or the Asian tropics. For example, you won’t often find a tropical African Anopheles in Northern Europe. But within each zone, you will find perhaps a handful of different Anopheles species, some of which are unreliable malaria carriers, while others are fabulous at it.

  It would be nice if the variety of local species of Anopheles depended on some unchanging factor in the landscape, so we could simply avoid those places where the worst mosquitoes lived, just as we avoid living around, say, alligators or grizzly bears. Unfortunately, the peculiar mix of species in a given locale depends mostly upon a rather more mutable part of the landscape. The impregnated female mosquito must lay her eggs in bodies of water where they will hatch and feed on whatever debris floats by. The larvae’s survival depends on being deposited in an amenable place to which its kind has been specifically adapted. Some thrive in salty water; others must have fresh. Some require shade; others, sun. Some demand flowing waters; others, stagnant.

  The trouble is that the hydrology of puddles, streams, and ponds is one of the more mercurial aspects of the environment, vulnerable to any number of disruptive influences. We remake mosquitoes’ microhabitats ourselves, mindlessly and routinely, by felling a few trees or digging a few holes. In so doing, we alter the temperature, rate of flow, and chemical composition of puddles, streams, and pond edges. To us these small alterations seem like nothing. But for the mosquitoes, they are the difference between life and death.

  When the landscape is static, there’s only so much of each kind of larval habitat available, and the mix of local Anopheles species can thus remain relatively stable. All things being the same, the larvae of the dominant species will fight off any intruders, and its populace is likely to become increasingly adapted to its specific niche. Once malaria transmission is established, the local people will, too, in time grow accustomed to the parasite, acquiring a patina of partial immunity. A relatively stable malarial ecology is established. Mortality declines.

  But when the local malaria ecology twists and turns, new opportunities arise for the malaria parasite. Perhaps the local vector’s habitat is extended, allowing the parasite to reach into new human populations. Or maybe the local vector is crowded out and a new, more efficient Anopheles population takes root, allowing the parasite to penetrate the local humans in more robust ways. Then the parasite’s gains are the local humans’ loss, for it can adapt much more quickly to the changed conditions than can the humans upon which it preys. In the lag between exposure to the new pattern of malaria transmission and the acquisition of immunity, the death toll rises.

  Take the Roman Empire. The founding of the ancient city of Rome upon the banks of the Tiber in 753 BC created a prime habitat for the European malaria vector, Anopheles atroparvus. The Tiber, an actively migrating stream back then, regularly flooded its banks, leaving behind scores of puddles and pools in which A. atroparvus’s young thrived.1 The Roman penchant for vegetable gardens, fountains, and impluvia provided even more mosquito nurseries. With an abundance of available larval sites and plenty of Romans to feast on, A. atroparvus abounded in Rome.2 By 200 BC, a stable malarial ecology had been established, with A. atroparvus regularly passing on P. vivax parasites to the locals.3

  Luckily for Rome, while A. atroparvus ably carried P. vivax parasites, that mosquito wasn’t a reliable carrier of P. falciparum. Unlike P. vivax, P. falciparum ’s survival depends on continuous transmission, without which it dies out, trapped inside its host. A stream of P. falciparum parasites regularly trickled into the Italian peninsula, in the bodies of traders and slaves from Africa. But A. atroparvus successfully foiled it before it took root. For one thing, the A. atroparvus mosquito is as attracted to animals for its blood meal as it is to humans, so its carriage of malaria to the correct host is not the most reliable. Every now and again, a falciparum-infected A. atroparvus mosquito would deposit P. falciparum parasites inside a cow or horse, which meant certain death for the parasite. Worse, A. atroparvus hibernates all winter. Once the cool weather arrives, it stops biting and repairs to some dark, warm corner for weeks at a time. For P. vivax parasites, which can go dormant, this wasn’t a problem. But pauses are a deal-breaker for P. falciparum. After a few weeks inside the body of a human or an insect without access to new blood, P. falciparum parasites disintegrate.4

  More reliable, nonhibernating, human-loving biters such as Anopheles labranchiae flit in North Africa, on the other side of the Mediterranean. Ancient Rome increasingly relied on imported grain from the second century onward. Stowaway A. labranchiae would have regularly arrived in Rome on the grain ships from North Africa, and were able travelers. While traders loaded the ships, rain showers might fill some broken clay jars with water, into which a passing female A. labranchiae might lay her eggs. The tiny ornamented pods, coated in a velvety pile, would balance upon the water’s surface with two air-filled floats shaped like fans on either side.5

  If conditions were amenable, by the time the wormlike larvae, with their giant eyes and spiky whiskers, hatched, they would have been in Rome.6 Nobody would have noticed the skittish, ascetic little pupae they became. They don’t eat anything; they have no mouths. If even so much as a shadow passes over them, they flip their tails and duck out of sight, rising to the surface again only to breathe. When the adult A. labranchiae emerges from the pupae, she is soft and wobbly. But after half an hour, her cuticle stiffens and she flies off to some still, dark corner. She can fly as far as eight miles in search of a meal. With the help of a strong wind, she could end up hundreds of miles away.7

  But Rome’s A. atroparvus effectively repelled such interlopers, and had already claimed all the best mosquito nurseries, those watery areas free of predatory fish. If any A. labranchiae mosquitoes successfully deposited a few eggs somewhere, they’d be fish food soon enough. If they dared lay claim to A. atroparvus turf, there’d be dire consequences. Anopheles actively guard their territory from encroachment by rival species, their larvae secreting deadly chemicals to kill off any newcomers that they don’t devour.8

  The ecology o
f malaria in early Rome was thus both stable and resilient. This helped strengthen the empire, for it meant that the Romans had ample opportunity to adapt to life with the parasite, and exercise an immunological advantage over foreign intruders who did not. Most powerfully, people across the Italian peninsula and around the Mediterranean developed genetic defenses against the worst ravages of the parasite. Genes that disrupted an enzyme called G6PD, required for normal functioning of red blood cells, emerged and spread. The defect impaired human bodies’ ability to repair oxygen damage, so that malaria-infected cells essentially poisoned themselves. (The main drawback: the peninsula’s famous fava beans could send G6PD-deficient Italians into a spiral of hemolytic anemia, a condition known as favism, after the bean.)9

  The Romans adapted culturally, too. They understood enough about the epidemiology of their malaria to minimize exposure to it. Ancient Roman scholars such as first-century BC writer Marcus Terentius Varro warned that animals too small to be seen (he called them bestiolae) entered the mouth and nostrils and caused horrible diseases.10 He recommended that Roman houses be built on high land, where the wind would blow the beasties away. Roman elites thus built their sumptuous villas in the mosquito-free hills. Even the peasants who worked the infested lands below the villas knew to avoid the sickly winds, building their houses with windows facing in, toward a central courtyard, rather than out into the breeze.11 The very worst mosquito-ridden regions, such as the rich wetlands of the Pontine marshes and the Roman Campagna, which ringed the metropolis, were abandoned to brigands, highwaymen, and the odd pallid peasant. Although these were the nearest and best agricultural lands, to avoid their malarious mosquitoes, the Romans (after a period of development) left them sparsely settled.12

  For the inevitable infections they suffered, the Romans devised a varied and fanciful welter of antimalarial therapies. The malarious might try some honeysuckle dissolved in wine to relieve their swollen spleens, or perhaps consume the liver of a seven-year-old mouse.13 They might, as the emperor Caracalla’s physician, Serenus Sammonicus, recommended, wear a piece of papyrus inscribed with a powerful incantation—“abracadabra”—around their necks as an amulet. Bolder souls might try Sammonicus’s other malaria cure: bedbugs eaten with eggs and wine.14 They might try waking at dawn three mornings in a row, facing a window, and shutting it suddenly while reciting a prayer, or, for a male sufferer, having intercourse with a woman just starting to menstruate.15 Prominent Roman physician Galen and medical scholar Celsus advocated energetic bloodletting. Finally, when all else failed, the Romans prayed for relief to the demon goddess of malaria, Febris, in three dedicated temples around the city.16

  Just as malaria immunity helped the Bantu spread and restrained European intrusion into malarious Africa, so Rome’s cultural and biological adaptation to chronic vivax malaria helped strengthen the city’s ability to repel outsiders. To enter the capital, the armies of malaria-free Northern Europe would have to spend days in the malarious swamps around the city, exposed to the bites of infected Anopheles. Unlike the regularly exposed Romans, the Northern Europeans had no tricks to help them minimize malarial feasts on their bodies. Time and again foreign armies fell prey to Rome’s malaria. “When unable to defend herself by the sword,” the poet Godfrey of Viterbo noted, “Rome could defend herself by means of the fever.”17

  And so, even as Julius Caesar lay in bed with malaria, his armies conquered lands far and wide, bringing booty and slaves to enrich Rome.18 Having forsaken its best farmland to malaria, ancient Rome could not feed itself, but the riches of conquest paid for grain, olives, fish sauce, and oil imported from North Africa. It paid for elaborate aqueducts, allowing wealthy Romans to move away from the most mosquito-ridden water’s edge.19 Until the environmental conditions that underlay Rome’s stable malarial ecology shifted, the malarious Roman Empire thrived.

  But building an empire required natural resources, and Rome’s oak forests suffered the brunt. As the peninsula was deforested, the usual changes occurred. Erosion intensified. As sheets of rainwater washed off the shorn hills and into the valleys below, the water table rose. Rivers flooded more easily. The plains grew marshy.20

  What this meant is that Rome increasingly harbored a new, uncolonized mosquito habitat, and at some point, stowaway A. labranchiae from North Africa must have found amenable spots unharassed by A. atroparvus and quietly laid their eggs.21 Adapting to Rome’s cool winters required a simple adjustment for the nonhibernating insects—spending the winter indoors, say, inside warm, dimly lit Roman homes, where they could continue to bite year-round.22 It wasn’t a big stretch. The behavior of Anopheles mosquitoes is not that rigid. We don’t know precisely when A. labranchiae made itself at home in Rome, but we do know that it did. In time, the mosquito established a foothold on the peninsula as well as on the islands of Sicily and Sardinia, which A. atroparvus had failed to colonize.23

  By the fifth century AD, Roman villagers were suffering horribly from P. falciparum outbreaks. The disease terrified them in a way that suggests the scourge had been previously unknown. Between 1988 and 1992, the archaeologist David Soren and his team from the University of Arizona excavated the remains of nearly fifty infant corpses from a fifth-century village near Rome called Lugnano. The infants had died in rapid succession and been buried hastily, in an ad hoc trash heap, entombed with mysterious offerings to pagan gods. Along with the bodies of their dead babies, the villagers had buried the torn-off jaw of a six-month-old puppy and the carcass of a dog split straight down the middle. They’d included the claws of ravens and singed honeysuckle branches. The hands and feet of the body of a two-year-old child had been weighed down with giant stones and tiles.24

  The carnage started to make sense when molecular biologists discovered the DNA of falciparum parasites inside the excavated bones.25 P. falciparum preys most prolifically on babies and young children, which would explain the predominance of dead babies at the site. After the first few infections, falciparum malaria spreads quickly—a single victim can infect one hundred others. Thus the quick succession of hasty burials. Honeysuckle was a known Roman salve for malarial symptoms. As for the mutilated dogs—well, if it was P. falciparum that killed the babies, the outbreak would probably have occurred in the heat of summer, when the waters of the Tiber running alongside the village receded, leaving behind a mess of puddle and marsh. Those long summer days were known in Roman times as the caniculares dies, the dog days, when the dog star Sirius disappears in the glow of the sun. And the keeper of infants’ souls, according to Roman mythology, was the goddess Hecate, who sailed through the heavens on a chariot pulled by the hounds of hell.26

  Making offerings to appease an enraged Hecate made sense in the face of a summer outbreak of an infant-slaughtering pathogen. Early medieval Romans had no other explanation for an illness that suddenly struck so many people at once. Their medical authorities considered sickness to be the result of idiosyncratic imbalances in the body. They had no concept for contagion. A curse cast by the pagan gods of their ancestors must have seemed the most reasonable explanation, the goddess Hecate the most likely culprit.27

  But the canine sacrifices also point to the terror the villagers must have felt. Practicing pagan rituals in that period risked serious political consequences. By the fifth century, Christianity had been the official religion of the Roman Empire for some two hundred years.28 The Church reserved special venom for the followers of Febris, and anyone caught wearing an amulet was to be executed.29

  It wouldn’t have been the fact of child deaths that scared the Romans. Generally speaking, fewer than half of the infants in early medieval Roman villages such as Lugnano survived childhood, and even the adults wouldn’t have expected to live past twenty years.30 More likely, the deadly epidemic was something novel, something they’d never seen before. As falciparum infection progresses, the symptoms of fever and chills become much more pronounced, and divergent from the usual vivax malaria to which the villagers were undoubtedly inured. Some
victims would have fallen into open-eyed comas and gone into convulsions. Such symptoms might well have struck the villagers as otherworldly, which would explain why they weighed down the body of one dead child with stones and tiles, as if to prevent the evil spirit that seemed to possess her from rising again.

  If the fifth-century falciparum outbreak in Lugnano was indeed new, its emergence in Rome coincided with a broader dissipation of the empire’s power. The fifth century found the empire weakened, under attack, and wasted by famine. In AD 401, for the first time in eight centuries, the city of Rome’s famous defenses were breached by Alaric and his Visigoth army.31 Fifth-century Romans had to survive on shipments of food from North Africa, a thin thread that northern armies severed simply by holding up the grain ships at sea, plunging Rome into famine.32 The elaborate villas that sat above villages such as Lugnano lay in ruins; villagers squatted in the rubble.33

  Historians still debate what triggered Rome’s decline. Was it the empire’s internal contradictions, the superior technology of its rivals, its trade deficits, its plagues and pestilences? Clearly, many things went awry. But the transformation of malaria from the fever that protected Rome to one that killed, occurring just around the time of Rome’s decline, surely exerted a demoralizing and destabilizing effect.

  As falciparum transmission became established, the troublesome but mild malaria season would have yielded to a year-round scourge, which struck foreigners and Romans with equal severity. P. falciparum would have laid bare the inadequacies of Roman medicine and mythology. Amulets and prayers might have seemed effective in the face of self-limiting vivax infections, for by probability alone, their use would have sometimes coincided with P. vivax’s natural cessation. Not so with P. falciparum infection. Its arrival, thanks to slow-moving ecological disruptions, shattered all the old certainties.