BIOLOGICAL PEST CONTROL: A HISTORY
E. F. Legner
Professor of Biological Control
University of California
Biological pest control might have been recognized circa 400 BCE in China with the correct interpretation of behavior and development of predators, but F. Redi in 1668 observed that arthropods do not arise by spontaneous generation (DeBach & Rosen 1991). Van Leeuwenhoek in 1700 proposed that parasitoids and pathogens might be essential to the natural control of pests. However, it was R. Réaumur in 1734 that suggested such organisms be used as a direct pest control tactic. He advised the release of lacewings in greenhouses for the control of aphids.
Earlier observations by ordinary farmers certainly led to an appreciation of the action of predators, as predation is obvious and easily viewed. Indeed, pest control was attained in Egypt by 2,000 BCE when humans kept cats to protect stored grain from rodents. In China citrus growers used Oecophylla smaragdina Fab. for the control of lepidopteran and coleopteran pests in 324 BCE. The ants build nests in trees and these were collected and sold to growers. In order to aid the foraging of ants, bamboo bridges were built between the citrus trees. DeBach (1974) observed this practice still being used in North Burma in the 1950s, and it continues to be used in China. Other efforts deployed general predators such as the mongoose, owls and other birds, toads, ants, etc.
Linnaeus also considered the use of predators for pest control (Höestadius 1974). The first successful importation of an organism from one country to another for biological pest control took place in 1762 with the introduction of the mynah bird from India to the island of Mauritius for control of the red locust Nomadacris septemfasciata (Serv.) (DeBach & Rosen 1991).
Insect parasitism was not recognized until the 17th Century when the Italian U. Aldrovandi in1602 observed the cocoons of Apanteles glomeratus (L.) being attached to larvae of Pieris brassicae L. (Bodenheimer 1931). He incorrectly believed that the cocoons were insect eggs, as he stated, "Twice have I also observed the cabbage caterpillar laying yellow eggs covered with delicate wool, and afterwards transforming itself into a yellowish pupa, marked with green and black. What appeared peculiar to me was that from these eggs emerged small winged animalcules, so small that they could barely be seen..."
Illustrations of parasitoids appeared in Holland by Johannes Goedaert (1662) in his book Metamorphosis et Historia Naturalis Insectorum. He noted, "Out of one caterpillar, which had pupated on June 12, emerged on the 30th the butterfly species.... But out of another caterpillar of the same species, which had pupated on July 13, emerged after pupation 82 small flies, as the reader can see in the figure added. Thus from one caterpillar a butterfly emerged and from the other 82 small flies."
The British physician Martin Lister suggested in letters published in the 1670-71 issue of the Philosophical Transactions of the Royal Society of London, that some insects lay their eggs in the bodies of living caterpillars and in 1685 he correctly interpreted Goedaert's observations, "The 82 flies that emerged from the pupa are the progeny of an ichneumon fly, which had gotten into the caterpillar in a manner that is still not entirely clear to me..."
Another 25 years was required before the cycle of parasitism was fully analyzed and described. The Dutch microscopist Antoni van Leeuwenhoek in a letter of 26 October 1700 to the Royal Society fully noted that some of the berry plants in his garden in Delft had more flowers than usual. He also observed that the "black flies" on these plants were more numerous than in other years. He dismayed that the offspring of so many blackflies would completely devastate his berry plants. After studying the mouthparts of the "blackflies" he concluded that they would not be able to eat the leaves, "These last flies that I caught were all females, and had their eggs in them; from whence I more strongly concluded that the black flies did the trees no harm; for if they had laid their eggs on the trees, and that all their eggs had produced so many living insects, there would not, I am positive, be one leaf or any fruit remaining on the trees." Leeuwenhoek strongly denied the theory of spontaneous generation, a hotly debated topic during his time. He continued with, "I shifted these flies into another glass tube, where I had before put six green lice [aphids], which I had taken from the leaf of a currant-tree... These flies, as soon as ever they came near the said lice, brought the hinder part of their body, which was pretty long, between all their feet, and stretched their body far out, and their tail making a kind of semicircle with the rest of the body, stood out beyond their head, and in this manner they insinuated their tail into the bodies of the worms, and this the flies did in a short time to all the worms they came near to; but that which was most remarkable in this action was that in this conjunction they never touched the lice, either with their feet or bodies, so that they often essa'd to approach the creatures, in order to thrust in their tails into their bodies, and could not effect it; nay, one would say they were so afraid of these lice as if they would have devoured them; and as they entered the bodies of the lice they made a trillende [shivering] motion of shaking with their tail, which came to be done so that they might thrust it in further."
"Now, as the flies remained but two days alive without copulation, as ever I observed, whereas the green lice lived seven or eight days, I though not otherwise but that the flies by that insinuation of their tails into the bodies of those lice, did withal convey their eggs in the same time, and that from those eggs young worms should have been produced, which having received their nourishment and increase from the bodies of the lice, should be changed again into a fly, but the green lice died, and for the most part dried away. Not content with this observation I got together again 25 dead lice, all of which in their bellies a worm, or else a fly newly changed, for I saw through the skin of some of the lice, living flies, which flies I took out alive from the bodies of some of those green lice which I opened on purpose... Now if we observe the wonderful formation of such a small creature, and how such a fly is produced, and then consider that the worm which is changed into the fly, and we imagine that such a thing will not happen, unless the worm that comes out of the egg of the fly makes use of another creature for its food, we must remain perfectly amazed."
From this description it can be concluded that what van Leeuwenhoek very exactly described the behavior of a parasitoid of aphids. The illustration, which was published with the letter, is of such good quality that the insect could easily be determined to be Aphidius ribis Haliday, a parasitoid of the aphid Cryptomyzus ribis (L.). Thereafter in the 18th Century, knowledge of parasitoids rapidly increased.
Silkworm diseases were recognized as early as the 18th Century, although earlier the Greeks and Romans were aware of diseases of bees. Many publications in the 16th, 17th and 18th Centuries dealt with diseases of silkworms, silk being a very important industry at the time. Vallisnieri was the first to mention the muscardine disease of silkworm. De Reamur (1726) described and was the first to illustrate a fungus, Cordyceps, infecting a noctuid larva. The microbial nature of these diseases was not yet realized. From William Kirby’s chapter on "Diseases of Insects" (Kirby & Spence 1815) we learn that it was recognized that true fungi grew in the bodies of insects as saprophytes and possibly as parasites. Agustino Bassi (1835) first experimentally demonstrated that a microorganism, Beauveria bassiana(Bal. Vuill) caused an animal disease, namely the muscardine disease of silkworms, and he suggested that microorganisms be used for insect pest control. Later in 1874, Louis Pasteur advised the use of microorganisms against the grape phylloxera in France. These suggestions did not result in practical application. Elie Metchnikoff tried to develop biological pest control for the wheat cockchafer, Anisopilia austriaca Herbst, a serious pest of cereal crops in the area of Odessa, Russia. In 1879 he published a paper on Metarrhizium anisopliae (Metsch) Sorok., and his experiments led to the conclusion that the fungus, when mass-produced and properly introduced in the field, might result in effective control. Based on Metchnikoff's work, Metarrhizium was mass-produced in 1884 in the Ukraine, and the spores were tested in the field against a curculionid, Cleonus punctiventris Germ. in sugar beets.
Biological weed control did not begin until after 1850 (Goede 1978). The American Asa Fitch was the first to suggest biological control of weeds around 1855, when he observed that a European weed in New York pastures did not have American insects feeding on it. He suggested that importation of European insects feeding on this weed might solve the problem. The first practical attempt dates from 1863, when Dactylopius ceylonicus (Green), was distributed for cactus control in southern India after they had been observed to decimate cultivated plantings of the prickly pear cactus, Opuntia vulgaris Miller, in northern India (Goeden 1978). In 1865, the first successful international importation for weed control took place, when this same insect was transferred from India to Sri Lanka, where in a few years widespread populations of the same cactus, O. vulgaris, was effectively controlled.
During the 19th Century taxonomy rapidly developed and many biological studies of natural enemies were made. Practical ideas and tests about application of biological pest control gradually advanced. Erasmus Darwin, the grandfather of Charles Darwin, published Phytologia, a book on agriculture and gardening in 1800, in it stressing the role of natural enemies in reducing pests. Moreover, he advised that aphids in hothouses be controlled by artificial use of predaceous syrphid fly larvae. Augmentation of ladybird beetles for control of hop aphids in the field and aphids in greenhouses was also recommended by Kirby & Spence (1815).
By 1850 with the westward expansion of agriculture biological pest control obtained full attention in the United States, where imported pests were taking a large toll of both domestic and imported crops. Entomologists, such as Asa Fitch, C. V. Riley and Benjamin D. Walsh, suggested the importation of natural enemies from their homeland. It was C. V. Riley (1893) who organized the first intra-state parasitoid transport when he sent parasitoids of the plum curculio, Conotrachelus nenuphar (Herbst), to different localities in Missouri [probably a wasted effort]. Riley was also the first to propose conservation of parasitoids of the rascal leafcrumpler of fruit trees, Acrobasis indigenella [???], by collecting larvae in their cases in mid-winter and then placing them away from the tree far enough that the larvae could not reach the trees anymore, but the parasitoids emerging from parasitized individuals in springtime could easily do so. Also, in 1873, Riley stimulated the first international transfer of an arthropod predator by sending the predatory mite Tyroglyphus phylloxerae Riley to France for control of the grape phylloxera, Daktulosphaira vitifolii Fitch. It established but did not result in effective control. The first international shipment of a predatory insect took place in 1874, when aphid predators, among which Coccinella undecimpunctata L., were shipped from England to New Zealand and became established. The first international transfer of parasitic insects was Trichogramma from the United States to Canada in 1882. The first intercontinental parasitoid shipment took place in 1883, when Riley organized the shipment of Apanteles glomeratus (L.) from England to the United States for control of cabbage white butterflies. It was just another six years before the spectacular success with Rodolia cardinalis Muls. against the citrus cottony-cushion scale, Icerya purchasi Mask., took place, again under the direction of Riley.
Biological control expanded in the 20th Century when Harry S. Smith of the University of California redefined the host relationships of entomophagous insects (Smith 1916). This was followed by a half century of numerous successes worldwide (Bellows & Fisher 1999).
Integrated Pest Control
Integrated Control's future is very bright, especially with its new title "Integrated Pest Management," that is more generally understood by scientists and the public alike. There is no doubt expressed concerning the importance and value of the integrated control concept. But, much work remains in order to implement integrated control on a wider scale. A broad interdisciplinary approach is needed, pooling talents of research teams. This also means incorporating economic considerations.
There are special difficulties of establishing integrated control in crops where excessive demands for eye appeal as a measure of quality, are great. There are also great difficulties in grower and extension personnel education. Integrated control programs are complicated and in some instances require trained supervisors. Governments can take a more active role in stimulating development of integrated control by instituting advisory services for promoting its merits, supporting intensified research in ecology, systematics, population dynamics, and in the development of selective insecticides, attractants, repellents, etc. Governments would be wise to take over from the chemical industry the cost of the non-paying part of selective insecticide development. The conclusion is that we have a long way to go before integrated control gains widespread effective application (Pimentel et al 1991.
Particular problems exist for the integration of Insect Pathology. Ways must be found to better use microorganisms to control insect pests: mass production, dissemination, and in combination with insecticides and with entomophagous insects. However, Biological Weed Control's future is extremely optimistic if environmental groups concerned with endangered species can weigh the gains and detriments accurately. As there are over 1,000 introduced weed species in America, and only ca. two percent of weeds are presently targets for the technique, there are still relatively unlimited opportunities for future efforts. Great possibilities exist for the Biological Control of Medically Important Pests, especially where chemicals are not practical to apply (Legner & Sjogren 1984, Garcia & Legner 1999) The prospects of importation of natural enemies has just begun to be explored. Where importation has been done, results were often spectacular. The problem of financing this research is great since economic losses are not neatly tied to the problem. Local financing is available, but rarely is this adequate for importing exotic beneficial organisms.
I would like to acknowledge the assistance of Dr. Joop Van Lenteren with the Leeuwenhoek translation.
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