Silent Spring: 40th Anniversary Edition

16. The Rumblings of an Avalanche

IF DARWIN were alive today the insect world would delight and astound him with its impressive verification of his theories of the survival of the fittest. Under the stress of intensive chemical spraying the weaker members of the insect populations are being weeded out. Now, in many areas and among many species only the strong and fit remain to defy our efforts to control them.

Nearly half a century ago, a professor of entomology at Washington State College, A. L. Melander, asked the now purely rhetorical question, “Can insects become resistant to sprays?” If the answer seemed to Melander unclear, or slow in coming, that was only because he asked his question too soon—in 1914 instead of 40 years later. In the pre-DDT era, inorganic chemicals, applied on a scale that today would seem extraordinarily modest, produced here and there strains of insects that could survive chemical spraying or dusting. Melander himself had run into difficulty with the San José scale, for some years satisfactorily controlled by spraying with lime sulfur. Then in the Clarkston area of Washington the insects became refractory—they were harder to kill than in the orchards of the Wenatchee and Yakima valleys and elsewhere.

Suddenly the scale insects in other parts of the country seemed to have got the same idea: it was not necessary for them to die under the sprayings of lime sulfur, diligently and liberally applied by orchardists. Throughout much of the Midwest thousands of acres of fine orchards were destroyed by insects now impervious to spraying.

Then in California the time-honored method of placing canvas tents over trees and fumigating them with hydrocyanic acid began to yield disappointing results in certain areas, a problem that led to research at the California Citrus Experiment Station, beginning about 1915 and continuing for a quarter of a century. Another insect to learn the profitable way of resistance was the codling moth, or appleworm, in the 1920’s, although lead arsenate had been used successfully against it for some 40 years.

But it was the advent of DDT and all its many relatives that ushered in the true Age of Resistance. It need have surprised no one with even the simplest knowledge of insects or of the dynamics of animal populations that within a matter of a very few years an ugly and dangerous problem had clearly defined itself. Yet awareness of the fact that insects possess an effective counterweapon to aggressive chemical attack seems to have dawned slowly. Only those concerned with disease-carrying insects seem by now to have been thoroughly aroused to the alarming nature of the situation; the agriculturists still for the most part blithely put their faith in the development of new and ever more toxic chemicals, although the present difficulties have been born of just such specious reasoning.

If understanding of the phenomenon of insect resistance developed slowly, it was far otherwise with resistance itself. Before 1945 only about a dozen species were known to have developed resistance to any of the pre-DDT insecticides. With the new organic chemicals and new methods for their intensive application, resistance began a meteoric rise that reached the alarming level of 137 species in 1960. No one believes the end is in sight. More than 1000 technical papers have now been published on the subject. The World Health Organization has enlisted the aid of some 300 scientists in all pans of the world, declaring that “resistance is at present the most important single problem facing vector-control programmes.” A distinguished British student of animal populations, Dr. Charles Elton, has said, “We are hearing the early rumblings of what may become an avalanche in strength.”

Sometimes resistance develops so rapidly that the ink is scarcely dry on a report hailing successful control of a species with some specified chemical when an amended report has to be issued. In South Africa, for example, cattlemen had long been plagued by the blue tick, from which, on one ranch alone, 600 head of cattle had died in one year. The tick had for some years been resistant to arsenical dips. Then benzene hexachloride was tried, and for a very short time all seemed to be well. Reports issued early in the year 1949 declared that the arsenic-resistant ticks could be controlled readily with the new chemical; later in the same year, a bleak notice of developing resistance had to be published. The situation prompted a writer in the Leather Trades Review to comment in 1950: “News such as this quietly trickling through scientific circles and appearing in small sections of the overseas press is enough to make headlines as big as those concerning the new atomic bomb if only the significance of the matter were properly understood.”

Although insect resistance is a matter of concern in agriculture and forestry, it is in the field of public health that the most serious apprehensions have been felt. The relation between various insects and many diseases of man is an ancient one. Mosquitoes of the genus Anopheles may inject into the human bloodstream the single-celled organism of malaria. Other mosquitoes transmit yellow fever. Still others carry encephalitis. The housefly, which does not bite, nevertheless by contact may contaminate human food with the bacillus of dysentery, and in many parts of the world may play an important part in the transmission of eye diseases. The list of diseases and their insect carriers, or vectors, includes typhus and body lice, plague and rat fleas, African sleeping sickness and tsetse flies, various fevers and ticks, and innumerable others.

These are important problems and must be met. No responsible person contends that insect-borne disease should be ignored. The question that has now urgently presented itself is whether it is either wise or responsible to attack the problem by methods that are rapidly making it worse. The world has heard much of the triumphant war against disease through the control of insect vectors of infection, but it has heard little of the other side of the story—the defeats, the short-lived triumphs that now strongly support the alarming view that the insect enemy has been made actually stronger by our efforts. Even worse, we may have destroyed our very means of fighting.

A distinguished Canadian entomologist, Dr. A. W. A. Brown, was engaged by the World Health Organization to make a comprehensive survey of the resistance problem. In the resulting monograph, published in 1958, Dr. Brown has this to say: “Barely a decade after the introduction of the potent synthetic insecticides in public health programmes, the main technical problem is the development of resistance to them by the insects they formerly controlled.” In publishing his monograph, the World Health Organization warned that “the vigorous offensive now being pursued against arthropod-borne diseases such as malaria, typhus fever, and plague risks a serious setback unless this new problem can be rapidly mastered.”

What is the measure of this setback? The list of resistant species now includes practically all of the insect groups of medical importance. Apparently the blackflies, sand flies, and tsetse flies have not yet become resistant to chemicals. On the other hand, resistance among houseflies and body lice has now developed on a global scale. Malaria programs are threatened by resistance among mosquitoes. The oriental rat flea, the principal vector of plague, has recently demonstrated resistance to DDT, a most serious development. Countries reporting resistance among a large number of other species represent every continent and most of the island groups.

Probably the first medical use of modern insecticides occurred in Italy in 1943 when the Allied Military Government launched a successful attack on typhus by dusting enormous numbers of people with DDT. This was followed two years later by extensive application of residual sprays for the control of malaria mosquitoes. Only a year later the first signs of trouble appeared. Both houseflies and mosquitoes of the genus Culex began to show resistance to the sprays. In 1948 a new chemical, chlordane, was tried as a supplement to DDT. This time good control was obtained for two years, but by August of 1950 chlordane-resistant flies appeared, and by the end of that year all of the houseflies as well as the Culex mosquitoes seemed to be resistant to chlordane. As rapidly as new chemicals were brought into use, resistance developed. By the end of 1951, DDT, methoxychlor, chlordane, heptachlor, and benzene hexachloride had joined the list of chemicals no longer effective. The flies, meanwhile, had become “fantastically abundant.”

The same cycle of events was being repeated in Sardinia during the late 1940’s. In Denmark, products containing DDT were first used in 1944; by 1947 fly control had failed in many places. In some areas of Egypt, flies had already become resistant to DDT by 1948; BHC was substituted but was effective for less than a year. One Egyptian village in particular symbolizes the problem. Insecticides gave good control of flies in 1950 and during this same year the infant mortality rate was reduced by nearly 50 per cent. The next year, nevertheless, flies were resistant to DDT and chlordane. The fly population returned to its former level; so did infant mortality.

In the United States, DDT resistance among flies had become widespread in the Tennessee Valley by 1948. Other areas followed. Attempts to restore control with dieldrin met with little success, for in some places the flies developed strong resistance to this chemical within only two months. After running through all the available chlorinated hydrocarbons, control agencies turned to the organic phosphates, but here again the story of resistance was repeated. The present conclusion of experts is that “housefly control has escaped insecticidal techniques and once more must be based on general sanitation.”

The control of body lice in Naples was one of the earliest and most publicized achievements of DDT. During the next few years its success in Italy was matched by the successful control of lice affecting some two million people in Japan and Korea in the winter of 1945–46. Some premonition of trouble ahead might have been gained by the failure to control a typhus epidemic in Spain in 1948. Despite this failure in actual practice, encouraging laboratory experiments led entomologists to believe lice were unlikely to develop resistance. Events in Korea in the winter of 1950–51 were therefore startling. When DDT powder was applied to a group of Korean soldiers the extraordinary result was an actual increase in the infestation of lice. When lice were collected and tested, it was found that 5 per cent DDT powder caused no increase in their natural mortality rate. Similar results among lice collected from vagrants in Tokyo, from an asylum in Itabashi, and from refugee camps in Syria, Jordan, and eastern Egypt, confirmed the ineffectiveness of DDT for the control of lice and typhus. When by 1957 the list of countries in which lice had become resistant to DDT was extended to include Iran, Turkey, Ethiopia, West Africa, South Africa, Peru, Chile, France, Yugoslavia, Afghanistan, Uganda, Mexico, and Tanganyika, the initial triumph in Italy seemed dim indeed.

The first malaria mosquito to develop resistance to DDT was Anopheles sacharovi in Greece. Extensive spraying was begun in 1946 with early success; by 1949, however, observers noticed that adult mosquitoes were resting in large numbers under road bridges, although they were absent from houses and stables that had been treated. Soon this habit of outside resting was extended to caves, outbuildings, and culverts and to the foliage and trunks of orange trees. Apparently the adult mosquitoes had become sufficiently tolerant of DDT to escape from sprayed buildings and rest and recover in the open. A few months later they were able to remain in houses, where they were found resting on treated walls.

This was a portent of the extremely serious situation that has now developed. Resistance to insecticides by mosquitoes of the anophelene group has surged upward at an astounding rate, being created by the thoroughness of the very house-spraying programs designed to eliminate malaria. In 1956, only 5 species of these mosquitoes displayed resistance; by early 1960 the number had risen from 5 to 28! The number includes very dangerous malaria vectors in West Africa, the Middle East, Central America, Indonesia, and the eastern European region.

Among other mosquitoes, including carriers of other diseases, the pattern is being repeated. A tropical mosquito that carries parasites responsible for such diseases as elephantiasis has become strongly resistant in many parts of the world. In some areas of the United States the mosquito vector of western equine encephalitis has developed resistance. An even more serious problem concerns the vector of yellow fever, for centuries one of the great plagues of the world. Insecticide-resistant strains of this mosquito have occurred in Southeast Asia and are now common in the Caribbean region.

The consequences of resistance in terms of malaria and other diseases are indicated by reports from many parts of the world. An outbreak of yellow fever in Trinidad in 1954 followed failure to control the vector mosquito because of resistance. There has been a flare-up of malaria in Indonesia and Iran. In Greece, Nigeria, and Liberia the mosquitoes continue to harbor and transmit the malaria parasite. A reduction of diarrheal disease achieved in Georgia through fly control was wiped out within about a year. The reduction in acute conjunctivitis in Egypt, also attained through temporary fly control, did not last beyond 1950.

Less serious in terms of human health, but vexatious as man measures economic values, is the fact that salt-marsh mosquitoes in Florida also are showing resistance. Although these are not vectors of disease, their presence in bloodthirsty swarms had rendered large areas of coastal Florida uninhabitable until control—of an uneasy and temporary nature—was established. But this was quickly lost.

The ordinary house mosquito is here and there developing resistance, a fact that should give pause to many communities that now regularly arrange for wholesale spraying. This species is now resistant to several insecticides, among which is the almost universally used DDT, in Italy, Israel, Japan, France, and parts of the United States, including California, Ohio, New Jersey, and Massachusetts.

Ticks are another problem. The woodtick, vector of spotted fever, has recently developed resistance; in the brown dog tick the ability to escape a chemical death has long been thoroughly and widely established. This poses problems for human beings as well as for dogs. The brown dog tick is a semitropical species and when it occurs as far north as New Jersey it must live over winter in heated buildings rather than out of doors. John C. Pallister of the American Museum of Natural History reported in the summer of 1959 that his department had been getting a number of calls from neighboring apartments on Central Park West. “Every now and then,” Mr. Pallister said, “a whole apartment house gets infested with young ticks, and they’re hard to get rid of. A dog will pick up ticks in Central Park, and then the ticks lay eggs and they hatch in the apartment. They seem immune to DDT or chlordane or most of our modern sprays. It used to be very unusual to have ticks in New York City, but now they’re all over here and on Long Island, in Westchester and on up into Connecticut. We’ve noticed this particularly in the past five or six years.”

The German cockroach throughout much of North America has become resistant to chlordane, once the favorite weapon of exterminators who have now turned to the organic phosphates. However, the recent development of resistance to these insecticides confronts the exterminators with the problem of where to go next.

Agencies concerned with vector-borne disease are at present coping with their problems by switching from one insecticide to another as resistance develops. But this cannot go on indefinitely, despite the ingenuity of the chemists in supplying new materials. Dr. Brown has pointed out that we are traveling “a one-way street.” No one knows how long the street is. If the dead end is reached before control of disease-carrying insects is achieved, our situation will indeed be critical.

With insects that infest crops the story is the same.

To the list of about a dozen agricultural insects showing resistance to the inorganic chemicals of an earlier era there is now added a host of others resistant to DDT, BHC, lindane, toxaphene, dieldrin, aldrin, and even to the phosphates from which so much was hoped. The total number of resistant species among crop-destroying insects had reached 65 in 1960 .

The first cases of DDT resistance among agricultural insects appeared in the United States in 1951, about six years after its first use. Perhaps the most troublesome situation concerns the codling moth, which is now resistant to DDT in practically all of the world’s apple-growing regions. Resistance in cabbage insects is creating another serious problem. Potato insects are escaping chemical control in many sections of the United States. Six species of cotton insects, along with an assortment of thrips, fruit moths, leaf hoppers, caterpillars, mites, aphids, wireworms, and many others now are able to ignore the farmer’s assault with chemical sprays.

The chemical industry is perhaps understandably loath to face up to the unpleasant fact of resistance. Even in 1959, with more than 100 major insect species showing definite resistance to chemicals, one of the leading journals in the field of agricultural chemistry spoke of “real or imagined” insect resistance. Yet hopefully as the industry may turn its face the other way, the problem simply does not go away, and it presents some unpleasant economic facts. One is that the cost of insect control by chemicals is increasing steadily. It is no longer possible to stockpile materials well in advance; what today may be the most promising of insecticidal chemicals may be the dismal failure of tomorrow. The very substantial financial investment involved in backing and launching an insecticide may be swept away as the insects prove once more that the effective approach to nature is not through brute force. And however rapidly technology may invent new uses for insecticides and new ways of applying them, it is likely to find the insects keeping a lap ahead.

Darwin himself could scarcely have found a better example of the operation of natural selection than is provided by the way the mechanism of resistance operates. Out of an original population, the members of which vary greatly in qualities of structure, behavior, or physiology, it is the “tough” insects that survive chemical attack. Spraying kills off the weaklings. The only survivors are insects that have some inherent quality that allows them to escape harm. These are the parents of the new generation, which, by simple inheritance, possesses all the qualities of “toughness” inherent in its forebears. Inevitably it follows that intensive spraying with powerful chemicals only makes worse the problem it is designed to solve. After a few generations, instead of a mixed population of strong and weak insects, there results a population consisting entirely of tough, resistant strains.

The means by which insects resist chemicals probably vary and as yet are not thoroughly understood. Some of the insects that defy chemical control are thought to be aided by a structural advantage, but there seems to be little actual proof of this. That immunity exists in some strains is clear, however, from observations like those of Dr. Briejèr, who reports watching flies at the Pest Control Institute at Springforbi, Denmark, “disporting themselves in DDT as much at home as primitive sorcerers cavorting over red-hot coals.”

Similar reports come from other parts of the world. In Malaya, at Kuala Lumpur, mosquitoes at first reacted to DDT by leaving the treated interiors. As resistance developed, however, they could be found at rest on surfaces where the deposit of DDT beneath them was clearly visible by torchlight. And in an army camp in southern Taiwan samples of resistant bedbugs were found actually carrying a deposit of DDT powder on their bodies. When these bedbugs were experimentally placed in cloth impregnated with DDT, they lived for as long as a month; they proceeded to lay their eggs; and the resulting young grew and thrived.

Nevertheless, the quality of resistance does not necessarily depend on physical structure. DDT-resistant flies possess an enzyme that allows them to detoxify the insecticide to the less toxic chemical DDE. This enzyme occurs only in flies that possess a genetic factor for DDT resistance. This factor is, of course, hereditary. How flies and other insects detoxify the organic phosphorus chemicals is less clearly understood.

Some behavioral habit may also place the insect out of reach of chemicals. Many workers have noticed the tendency of resistant flies to rest more on untreated horizontal surfaces than on treated walls. Resistant houseflies may have the stable-fly habit of sitting still in one place, thus greatly reducing the frequency of their contact with residues of poison. Some malaria mosquitoes have a habit that so reduces their exposure to DDT as to make them virtually immune. Irritated by the spray, they leave the huts and survive outside.

Ordinarily resistance takes two or three years to develop, although occasionally it will do so in only one season, or even less. At the other extreme it may take as long as six years. The number of generations produced by an insect population in a year is important, and this varies with species and climate. Flies in Canada, for example, have been slower to develop resistance than those in southern United States, where long hot summers favor a rapid rate of reproduction.

The hopeful question is sometimes asked, “If insects can become resistant to chemicals, could human beings do the same thing?” Theoretically they could; but since this would take hundreds or even thousands of years, the comfort to those living now is slight. Resistance is not something that develops in an individual. If he possesses at birth some qualities that make him less susceptible than others to poisons he is more likely to survive and produce children. Resistance, therefore, is something that develops in a population after time measured in several or many generations. Human populations reproduce at the rate of roughly three generations per century, but new insect generations arise in a matter of days or weeks.

“It is more sensible in some cases to rake a small amount of damage in preference to having none for a time but paying for it in the long run by losing the very means of fighting,” is the advice given in Holland by Dr. Briejèr in his capacity as director of the Plant Protection Service. “Practical advice should be ‘Spray as little as you possibly can’ rather than ‘Spray to the limit of your capacity.’ …Pressure on the pest population should always be as slight as possible.”

Unfortunately, such vision has not prevailed in the corresponding agricultural services of the United States. The Department of Agriculture’s Yearbook for 1952, devoted entirely to insects, recognizes the fact that insects become resistant but says, “More applications or greater quantities of the insecticides are needed then for adequate control.” The Department does not say what will happen when the only chemicals left untried are those that render the earth not only insectless but lifeless. But in 1959, only seven years after this advice was given, a Connecticut entomologist was quoted in the Journal of Agricultural and Food Chemistry to the effect that on at least one or two insect pests the last available new material was then being used.

Dr. Briejèr says:

We need a more high-minded orientation and a deeper insight, which I miss in many researchers. Life is a miracle beyond our comprehension, and we should reverence it even where we have to struggle against it…. The resort to weapons such as insecticides to control it is a proof of insufficient knowledge and of an incapacity so to guide the processes of nature that brute force becomes unnecessary. Humbleness is in order; there is no excuse for scientific conceit here.