Part 2 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

The practice of various biological methods of insect pest suppression has gained increasing acceptance, indeed popularity, in very recent years. A number of stim• uli have led to this situation, not the least of which is the overall popular environ• mental awareness which followed the publication of Rachel Carson's Silent Spring in 1962. But, as we shall see, an elegant and complex concept like biologi• cal insect pest suppression does not gain stature and prominence overnight, nor does it spring full-flower from the mind of any single person. Historically, the growth of the discipline was slow and sometimes painful; it is studded with a few sparkling success stories, some disappointments, and many unheralded applica• tions that are highly successful, but doomed to obscurity because of that very success. Indeed, the results of a successful program of biological pest suppression are not very impressive unless the situation can be compared to that which existed previously. In the following three chapters we shall touch on some of the high• lights in the development of the ideas and practices of "classical" biological insect pest suppression-this is, the directed use of parasitoids, predators, and patho• genic microorganisms to reduce and regulate insect pest populations to subecon• omic levels. Some of the more recently developed aspects and agencies of biologi• cal insect pest suppression are dealt with in greater detail later (Part 4). The earliest observational, intuitive, and empirical work discussed in Chapter 2.1 led to the recognition and appreciation of some basic ecological principles and the theories of population dynamics discussed in Chapter 2.2. In Chapter 2.3, these and other ecological concepts are presented in their philosophical relationship to the classical practice of biological insect pest suppression.

2.1 Historical Development

2.1.1 Early History to 1888

To discover the origins of the practice that is today known as biological control one must look deeply into the dim reaches of human prehistory. Surely long before the rise of humankind and the first slow faltering steps in the development of agriculture, insects were subject to interaction with other inhabitants of the biosphere. Some of these interactions were beneficial to the individual insect (e.g. supplied nutriment, protection, or other advantageous symbiotic relations), and some were detrimental (e.g. competition, disease, predation). All such interactions were necessary, for if the species was to survive in nature it had to do so in concert with other organisms, producing neither too many nor too few individuals for a

H. C. Coppel et al., Biological Insect Pest Suppression © Springer-Verlag Berlin · Heidelberg 1977 Early History to 1888 15 sustained stable population in a given environment. A biologist known as Charles Darwin was later to recognize this process and discuss it in great detail. Entomophagy, then, existed from the appearance of the first insects. These small comparatively vulnerable animals fell prey to all manner of predators, parasites, and diseases, some of which came to depend on them entirely for food. No one knows with certainty when "the knowing man," Homo sapiens, first became cognizant of entomophagy by other animals, but early humans them• selves probably utilized insects as part of their own diet much as many primitive peoples do today. It seems reasonable to assume that the simple fact of predation was recognized at an early date, because man was himself sometimes competing with other insect predators for the same food source, but the more subtle ideas of parasitism probably remained beyond comprehension for hundreds of years. Some insect diseases produce such spectacular effects that even primitive man must have noticed them and perhaps compared them to the afflictions of larger animals, though we have no evidence of this observation (Steinhaus, 1956). The discovery of agriculture and its development during Neolithic times, about 10000 B.C., put humankind into very direct competition with insects for food. With the coming of crop raising and monoculture came a localized abund• ance of certain plant foods, and inevitably a localized increase in the abundance of pests to utilize them. We know that as agriculture progressed in sophistication a certain amount of selection took place in the varieties of crop plants grown. Most notably selected were strains giving greater yields through larger or more numer• ous seeds, fruits, or tubers, but other desirable qualities were probably also noted and encouraged. Thus the selection of crop varieties exhibiting resistance to disease and insect pests can be considered the oldest practical application of a type of biological pest suppression. Just as early man observed birds eating insects, and snakes eating rodents in the woods and fields, he must also have noted the proclivity of certain wild felines toward a diet of mice and rats like those which infested his stores of grain and other foods. And so, the domestication of the house cat by the ancient Egyptians may well have been encouraged in part by this useful habit, and may be consi• dered as a second very early attempt at biological pest suppression. We may now move from the realm of conjecture to the world of recorded facts. In the Bible we encounter the various plagues which befell Egypt, and in the first chapter of the Book of Joel a series of insect depredations is described which later disappear, illustrating the early recognition of the cyclical nature of pest populations. As with many other aspects of biology, the writings of the ancient Greek and Roman naturalists contain some of the earliest recorded information pertinent to the subject at hand (Smith and Secoy, 1975). A number of the classical philosophers had things to say about insects, but few are as valuable or accessible as the writings of Aristotle and Pliny (Marlatt, 1898). Within the masses of general observations and descriptions covering various aspects of insect study can be found early references to insect pathology. Aristotle (384-322 B.c.), in his Histo• ria Animalium, described the ravages of the wax moth to honeycomb, and suggests that it brings "disease into the swarm" (Steinhaus, 1956). He further describes other disease symptoms in bees which may be interpreted as a foulbrood condi• tion. Similarly the Roman author, Pliny (23-79 A.D.), recognized several disease 16 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression conditions in bees. In another part of the world another domestic insect, the silkworm, also suffered from various afflictions, some of which were recognized as early as 1000 A.D. (Steinhaus, 1956). In all of these instances, however, not much of real practical value was presented or suggested; the ancient naturalists and philosophers contented themselves with simple observation and description, and it was not until after the Dark and Middle Ages that anything substantially new was added to the body of practical knowledge concerning natural mortality in insects. We are aware of two notable exceptions to this statement. Although insect predation was observed and recognized for a long time, the idea of actually using predatory animals for agricultural pest control was slow to germinate. What is apparently the first known use of this method, which is true biological insect suppression in the modern sense, was the practice by Chinese citrus growers of introducing predaceous ants into their groves (Liu, 1939). An old Chinese book called "Wonders from Southern China," published about 900 A.D., speaks of the availability in the local markets of large yellow ants with long legs (probably Oecophylla smaragdina F.) used to protect oranges from "wormy" fruit. Another writer mentioned the same fact in the 1300s and as late as 1939 ant nests were still for sale in the markets of Canton. McCook (1883) commented on a Chinese newspaper report of the method, and discussed the possibilities of using these ants or native species for pest suppression in the United States. A second, and similar instance of early biological control was the practice of the date growers of the Mideastern country of Yemen, who moved colonies of beneficial ants to their groves from the mountains each year for insect pest suppression (Botta, 1841). It was not long after the reestablishment of intellectual activity in Europe that new and valuable observations on the natural history of insects began to appear. In the sixteenth and early seventeenth centuries the renewed interest in science resulted mostly in the repetition ofthe beliefs of the ancients supplemented in part by original observation. Names like Gesner, Thomas Mouffet, and Aldrovandi characterize the times. Mouffet's 1heatrum Insectorum (which included Gesner's work) was published posthumously in 1634, and was the first book written exclu• sively about insects. The book discussed or figured such things as diseases and parasites of bees and a nematode-infected silkworm (Ordish, 1967). Although Mouffet's book was the first book written on insects, Ulysses Aldrovandi's De Animalibus Insectis was the first volume published on the subject in 1602. It summarized all the material previously written on insects and included the first published record of insect parasitism. An attack of the gregarious braconid paras• itoid, Apanteles glomeratus (L.), on the cabbage butterfly, Pieris rapae (L.), was shown, but misinterpreted by Aldrovandi, who thought the conspicuous parasi• toid cocoons were insect eggs. In 1668, the Italian, Francesco Redi, described the same phenomenon and also parasitism of aphids by an ichneumon "fly." Redi also deserves credit for disproving the doctrine of spontaneous generation of life from nonliving material, but it was not until 1706 that Vallisnieri correctly inter• preted all of these early observations on insect parasitism. The literature of the eighteenth century produced numerous other references to insect predators and parasitoids as naturalists began to question the works of antiquity and investigate the living world for themselves. In 1701 the great Dutch Early History to 1888 17 microscopist, van Leeuwenhoek illustrated and discussed a parasitoid of a willow sawfly (Doutt, 1964). Considering the level of sophistication of science at the time, the illustrated treatments of insect natural history by Goedert, De Geer, Bonnet, Geoffroy, and Reaumur are excellent in their execution. Particularly remarkable for its usefulness and accuracy is the work of Rene Reaumur (1734) who, perhaps more than any of the others, advanced the idea of biological insect pest suppres• sion. In his Memoires pour servir a L'histoire des Insectes he gave probably the earliest published recommendation for biological pest suppression when he sug• gested introducing the eggs of "aphidiverous flies" (i.e. lacewings) into green• houses to keep them free of aphids. Reaumur also noted a nematode parasite of bumble bees and included a chapter with figures of parasitized caterpillars. As early as 1726 he had described the so-called "Chinese plant worm" which was no doubt a lepidopterous larva infected with a Cordyceps fungus (Steinhaus, 1956). Most of the early naturalists were what we would today call ecologists, and this outlook allowed them to view pests with an inevitable inclination toward biological control. A quotation from Reaumur (1736) makes the point clear. People dislike caterpillars and if they were master would destroy them all on the spot. A moment's reflection of our true interest would nevertheless stop this hatred. We like to see the trees in our gardens and woods covered with leaves: we like to see birds, whose song and plumage delight us, in these same trees. We should be careful then not to ... kill all the caterpillars and deprive the greater part of these birds of their food. No doubt everything is very well arranged, but we do not see the relationships which so many different kinds of life have with each other ... In supposing ourselves to be the center of the universe, and every• thing to be in relation to ourselves, as we like to think, we are unable to perceive the less immediate but useful functions exercised by certain creatures whom we know by their direct, and possibly harmful, nearby effects. De Geer is reported to have said in the 1760s that "we shall never be able to guard ourselves against insects but by means of other insects" (Weiss, 1936). One other notable European biologist of the eighteenth century deserves special men• tion for his contributions to the development of biological control. Besides his great interest in systematics, Carolus Linnaeus was also an astute observer and ecologist whose second love was insects (Usinger, 1964). Following the thoughts of Reaumur (and under the pseudonym of C. N. Nelin), Linnaeus proposed con• trolling orchard pests with the introduction of the predaceous ground beetle, Calosoma sycophanta (L.). He actually carried out a test of the method by captur• ing Calosoma and other species of carabids in the forest and moving them to the orchard. A lady beetle, green lacewings, and a parasitic wasp were also recom• mended for suppression of aphids. As early as 1760, Linnaeus was enunciating the idea of the "balance of nature," observing that "phytophagous insects are assigned to others which destroy them if they become too numerous," and "thus there is a war of all against all." While most of this early activity took place in Europe, some discussion of biological pest suppression of sorts was taking place in the New World as well (Weiss, 1936). As early as 1771, recommendations were made "on the time of sowing pease, so as to preserve the crop from being Wormeaten." Destruction of grain stubble soon after harvest was suggested for Hessian fly control in 1792. With his original description of the spring cankerworm, Paleacrita vernata (Peck), W. D. Peck (1795) also mentioned natural control factors, including two impor- 18 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression tant species of birds and a disease, "deliquium," which was probably caused by a virus. Again, in 1800, Peck noted an egg parasitoid of the pear slug, Caliroa cerasi (L.). Mitchill (1799) suggested scraping all loose bark ofT the trees to destroy overwintering sites and expose female cankerworm adults to wind and bird pre• dation. There was even this strange recommendation for control of ants on plan• tations: "A small quantity of human feces, when placed in their hills, will not only destroy great numbers, but expel the rest from their habitations" (Weiss, 1936). Meanwhile, in a project that was ahead of its time by 100 years, the first international movement of a predator for insect pest suppression was accom• plished in 1762 (Moutia and Mamet, 1946). The red locust, N omadacris septemfas• ciata Serville, was one of the most persistent pests of sugarcane from the begin• ning of agriculture on the island of Mauritius in the Indian Ocean. In 1762, the mynah bird, Acridotheres tristis L., was introduced from India with the purpose of locust control. The idea seemed to succeed, as the problem caused by N omada• cris gradually decreased until, by 1770, the insect was no longer a serious pest. The sixteenth, seventeenth, and eighteenth centuries were characterized by increased scientific thought and, progessively, by more and more original obser• vation and experimentation. Simple observation and description of individual occurrences of insect parasitism, predatism, and disease were one necessary step in the development of the idea of biological pest suppression, but the recognition of a second important concept was essential for the practice to become viable. It was not until the nineteenth century that the potential importance of the various mortality agents in pest population suppression was fully realized. True, there had been the domestication of the cat, the forward looking recommendations of Reau• mur and Linnaeus, and the mynah bird introduction to Mauritius, but the con• troversial writings of Thomas Malthus on population problems and the subse• quent stimulation of Charles Darwin by these ideas were important factors in the final synthesis of the philosophy of biological control and its widespread dissemi• nation. Dr. Erasmus Darwin, grandfather to Charles, suggested that hothouses could be kept free of aphids with coccinellid beetles, and, in his Phytologia (1800), made an early recommendation for transfer of beneficial organisms between countries when he suggested infecting British water rats with tapeworms from American rats. He also observed that cabbage caterpillars would be far more destructive were not "half ofthem annually destroyed by a small ichneumon-fly." In America, a number of amateur entomologists were adding more informa• tion to what was known about entomophagous insects and diseases. Mitchill (1823) discussed various parasitic animals including Hymenoptera from insects. Jacob Cist (1824) published one of the first American records of a Cordyceps infection from a cockchafer. The egg and pupal parasitoids of the Hessian fly were discussed by Herrick (1840), who also published several notes on a Platygaster egg parasitoid of the cankerworm. And a questionably practical suggestion was made by a Philadelphia physician, Joseph Leidy, in 1862, to introduce into the public squares "a few turkeys, guinea fowls, and chickens which destroy all insects that come within their reach" (Weiss, 1936). Other, more practical, suggestions were appearing with increasing frequency in the European literature. Lady beetles received much acclaim. Kirby and Spence (1867) recommended them and actually used them for aphid control. Olliff Early History to 1888 19

(1891) claimed they had been in use for perhaps centuries by hop growers in South England who even purchased them in times of scarcity from women and children collectors. The German entomologist, G. L. Hartig, in 1827 gave instructions for holding parasitized caterpillars in cages from which the emergent parasitoids could escape to continue their beneficial activities in the adjacent woods. Another German forest entomologist, Ratzeburg, called attention to the importance of parasitoids in suppressing forest insect populations in his Ichneumon der Forestin• sekten (1844), but thought that man could do nothing to expedite the process. In Austria, the naturalist, Vincent Kollar (1840), published a useful Treatise on In• sects in 1837 at the authorization of Emperor Francis I. The book was mainly intended to familiarize the general public with harmful insects, and understanding the life history of pests was stressed as the key to effective control. Kollar suc• ceeded well in his aim by providing careful discussions of the natural history of over 120 species. Practical information on control practices was sparse outside of recommendations for various mechanical methods, but in a section on Means of Defense Against Noxious Insects he showed a clear understanding of the impor• tance of parasitoids and predators in "circumscribing the too great increase of certain insects." He discussed bats, and other useful insectivorous mammals, from moles and hedgehogs to squirrels and witd swine. Birds were of still more impor• tance and Kollar suggested legal protection for them and the mammals. Finally, beneficial insects were seen to have a prime role in pest suppression, and several groups were enumerated, including a highly accurate synopsis of the life history of a parasitic hymenopteran. Kirby and Spence (1867), in England, also recognized the importance of natu• ral enemies and natural control: "The great agents in ... keeping the noxious species within proper limits are other insects ... To them we are indebted ... that our crops and grain, our cattle, our fruit and forest trees ... are not totally destroyed." They described various predatory wasps, lacewing larvae, syrphids, and lady beetles for aphid control. They were aware of the usefulness of ichneu• monids, chalcids, parasitic Diptera, carabids, cicindellids, mantids, reduviids, dragonflies, and spiders. A practical suggestion made, especially in those times, was to "extirpate" bed bugs from a room in which they were numerous by releasing six or eight individuals of the predatory bug, Pentatoma bidens, and closing them in for several weeks. A number of studies on the biological aspect of insect population regulation were published in Russian between 1870 and 1890 including work on parasitoids and predators by Porchinskii, Keppen, and Lindeman (Chesnova, 1968). Boisgiraud, in France, claimed success in suppressing gypsy moth numbers on roadside poplars by collecting and releasing the predatory beetle, C. sycophanta. He also used a predaceous staphylinid beetle in his own garden to reduce earwig populations (Howard, 1930). In Italy, a prize was offered in 1845 for new, success• ful developments in the use of predaceous insects for pest suppression. Antonio Villa collected the Gold Medal for his experiments in controlling phytophagous pest insects in his garden with carabid and staphylinid beetles (Silvestri, 1909). He also presented a list of beneficial insects and admonished farmers not to destroy insects indiscriminately, but instead to distinguish between beneficial and harmful species. Other Italian workers of the period were Camillo Rondani, a systematist, who provided valuable host information for the parasitic insects he studied; T. 20 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

Bellenghi, a forward looking biologist, who once said, "Entomological parasitism has a future, and in it more than in anything else Italian agriculture must put its faith" (Howard, 1930); and Agostino Bassi, a pioneer insect pathologist, who first demonstrated the fungal nature of the muscardine disease of the silkworm in 1835 (Steinhaus, 1956). By the mid-1800s, the ever increasing accumulation of knowledge regarding parasitoids, predators, and disease was beginning to crystallize in the minds of certain members of the scientific community. As early as Linnaeus' time, food chains were recognized, and now the realization offood webs, ecosystems, and the "struggle for existence" was taking place. Of the many naturalists and early ecologists who were putting the pieces together into a coherent general idea called "the balance of nature," two names stand out: George Russell Wallace and Charles Darwin. The landmark ideas that these two workers presented to the world were in large part understood and reiterated by entomologists of the day. A particularly significant contribution was that of another Englishman, John Curtis, whose Farm Insects (1860) was an exhaustive treatment of the ecology of various agricultural pests, and included repeated emphasis on the function of parasitoids and predators in crop protection. As we have seen, most of the basic observations and philosophical elements leading toward the final emergence of the practice of biological control were developed in the Old World. The ultimate fusion of these ideas seems to have depended in the end, however, on a particular agricultural situation which oc• curred in America. Agriculture developed rapidly in the New World with its vast expanses of fertile soil and beneficial climate. Settlers obtained excellent yields for several seasons from exotic crops brought from their homelands and elsewhere. Then, suddenly a plague of insect pests would appear and destroy the crop year after year. Many of these pests were not new to the farmers, for they had been present in European fields; however, the explosive pest populations and subse• quent devastation were not characteristics familiar to them. The question of the differences between the two situations logically arose, and was addressed by a number of entomologists. It appears that the first New York State Entomologist, Asa Fitch, was the earliest worker to correctly analyze the problem and propose a cure, thus becom• ing the first to suggest international transfer of beneficial insects for pest suppres• sion (Doutt, 1964). Discussing the problems caused by an introduced European species of wheat midge, Sitodiplosis mosellana (Gehin), Fitch (1861) wrote: "It was after the disastrous results of the harvest of 1854, that ... I became persuaded that we had not any parasites, or at least any genuine and efficient parasites of the midge in this country, and that our only effectual remedy for this insect was to import these, its natural destroyers, from Europe." Fitch took it upon himself to write to John Curtis in England, and after explaining the problem and proposed methods for its solution, requested aid in obtaining parasitized host material. The idea received considerable discussion in England and was apparently considered promising, but as is so frequently the case with proposed plans for biological pest suppression, no funding was made available to finance the project, and as a result, no parasitoid transfers occurred. Strong support for Fitch's ideas was expressed in the state of Illinois by another prominent entomologist of the day, Benjamin Early History to 1888 21

Walsh. Throughout the 1860s, in a distinctive and wry style, he advocated the importation of parasitoids from Europe to suppress the ravages of various intro• duced pests, but to no avail. For example, in 1866 he concluded an article on the subject with the statement: "The principle is of general application; and whenever a Noxious European Insect becomes accidently domiciled among us, we should at once import the parasites and Cannibals that prey upon it at home." It was not until the following decade, however, that anyone made an effort to carry through on such suggestions. Surprisingly, although the idea of international transport of beneficial arthro• pods was first proposed to aid American agriculture, France was the country to which the first shipment was made, and that shipment originated in America. A promising young entomologist from Missouri, C. V. Riley, had discovered a pre• daceous mite, Tyroglyphus phylloxerae Riley, attacking the grape phylloxera, which was then (1873) a serious threat to the wine industry of France. The insect was of American origin, and so Riley cooperated with French workers Planchon and Foex, by sending them living mites as a potential controlling influence on phylloxera populations. The mites became established in their new home, but were unsuccessful in significantly reducing the pest population (the problem was later solved through the use of resistant host material sent from America). Riley was greatly influenced by the ideas of Fitch and Walsh, and, in 1870, was appar• ently the first to purposefully move parasitoids from one locality to another (Riley, 1893; Doutt, 1964), by transferring enemies of the plum curculio, Cono• trachelus nenuphar (Herbst), from Kirkwood, Missouri, to other parts of the State. Others soon followed suit, notably LeBaron and Howard in the United States, and DeCaux in France (Howard, 1930). Other early international transfers of beneficial insects included the movement of aphid enemies from England to New Zealand in 1874 with uncertain results (Doutt, 1964), and the first parasitoid introduction to Canada in 1882 by Saunders (1882). Saunders obtained specimens of the egg parasitoid, Trichogramma minutum (Riley), from New York state and released them near eggs of the imported currantworm, N ematus ribesii (Scopoli), in Ontario gardens (Baird, 1956). Finally, in 1883, the United States was the recipient of a beneficial insect, some 30 years after Fitch first recognized the usefulness of the technique. In fact, the successful importation of A. glomeratus by Riley (by this time with the United States Department of Agriculture) was the first intercontinental transfer of a parasitoid for biological control. The European braconid wasps, in time, became a valuable part of the parasitoid complex of the imported cabbage worm, P. ra• pae, in America (Riley, 1893). While these early experiments in the introduction of beneficial insects were in progress, another aspect of classical biological control was also developing. The Italian microbiologist, Agostino Bassi, is credited by Steinhaus (1956) with being the first worker to (somewhat indirectly) suggest employment of microbes for insect pest suppression in 1836. Louis Pasteur, in France, was more definitive in his suggestion (1874) for use of the protozoan causing pebrine disease in bees against the grape phylloxera, or, alternatively, to search for a fungus disease for the same purpose. In the same year, the great American entomologist, LeConte (1874), discussed "a new system of checks" for use against insect pests, among 22 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression them the production, introduction, and communication of diseases. This was the first definite and broadly based proposal of its kind to appear in the English language (Steinhaus, 1956). Later (1879), a German-American entomologist, H.A. Hagen, proposed the use of "beer mash or diluted yeast" applied with a sprinkler to initiate epizootics of insect disease, and in that same year, Comstock, Riley, and Burns all experimented with the method. Using commercial yeast preparations on caged test insects these workers and several others were notably, and understand• ably, unsuccessful in obtaining disease infections, since commercial yeast is not an insect pathogen. Only Burns noted high mortality in his experimental animals, and examination by Hagen confirmed the cause of death to be "yeast fungus in quantity." Such mortality, however, could only have resulted from contamination by true pathogenic microorganisms or some sort of coincidence. Despite the misinterpretation of the experiments, the fact remains that these men perceived and promoted the cause of microbial control within the limits of the knowledge of the day (Steinhaus, 1956). Meanwhile, in Europe, the Russian zoologist, Metchni• koff, was concerning himself with damage to cereal crops by the wheat cockchaf• er, Anisoplia austriaca Herbst. Noting the large oscillations in pest populations from year to year, he concluded that such variations were the result of three distinct diseases. One of these was caused by the "green muscardine" fungus, now known as M etarrhizium anisopliae (Metchnikoft) Sorokin. Metchnikoff found other insects susceptible to the disease, advocated its production and use for control of pests, and propagated the fungus artificially (Metchnikoff, 1880). By 1884 a pilot plant operation was producing Metarrhizium spores in commercial amounts (Krassilstschk, 1888). Although field tests with the spore preparations were very encouraging, the project was soon discontinued for indeterminate rea• sons. One fact that was apparent to many entomologists of the later part of the nineteenth century was the predominance of introduced species of insects in any list of important pests. For instance, Saunders (1878), in his presidential address to the Entomological Society of Ontario in 1878, dealt with the subject, enumerat• ing a group of important injurious species originating from Europe. This was doubtless due, he said, to the absence of the numerous parasitoids which preyed upon them in their native home, urging a special effort be made to transfer the beneficial insects to Canada. Similarly, Howard (1898) found that of the 73 most important "first class" insect pests in the United States at that time, 37 were imported, 6 of unknown origin, and 30 were native. He made a plea for stringent legal quarantine control measures. Riley (1893) cautioned against overoptimism in the introduction of beneficial insects from abroad, citing the probability that not all would match the success of the recent vedalia beetle project. As mentioned previously, Riley had been involved in the first international transfer of a beneficial arthropod, sending a predatory mite to France for grape phylloxera, and the first intercontinental importation of a parasitoid for biologi• cal control purposes, the introduction of A.glomeratus against the imported cab• bage worm. But, it was not until the eminently successful introduction of the coccinellid beetle, Rodolia cardinalis (Mulsant), from Australia to California un• der his direction, that Riley gained major stature, and biological insect pest suppression was put on sound footing. Middle History to 1940 23

2.1.2 Middle History to 1940

We have seen the development of the theory of biological insect pest suppression from its origin in the observations of prehistory and the ancient philosophers to the early practical experiments of the mid and late nineteenth century. The obser• vations accumulated gradually, and the ideas and theories they sowed germinated and grew eventually into a substantial philosophical base which is now frequently referred to as "classical biological control." A new era was about to dawn. Like a living growing plant, the idea flowered in the minds of a number of entomologists in the nineteenth century, and in 1888 bore its first influential fruit-the spectacu• lar success in controlling the cottonycushion scale in California. The fascinating story of the introduction of the vedalia beetle to California citrus groves has been recounted several times (Riley, 1893; Howard, 1917, 1930; Doutt, 1964) and is universally acknowledged to overshadow all previous efforts in its effect on the practice of applied entomology. At the risk of adding still another repetition of the story we will touch on the highlights of the event because of its historical significance to biological insect pest suppression. As early as 1882, a special committee of the California Horticultural Board was appointed to consider ways of dealing with the cottonycushion scale, Icerya purchasi Maskell, which was starting to threaten the fledgling citrus industry with disaster. C. V. Riley at the USDA in Washington, DC, was also considering the problem, having first noticed the scale in 1872. By 1886, he had two field agents, D. W. Coquillet and Albert Koebele, working in California to help him accumu• late information, and when he addressed a Fruit Growers Convention at River• side in 1887, Riley's assessment of the situation provided the hope that the grow• ers were seeking. He recognized that Icerya was an introduced pest which had probably originated in Australia, and that a notable lack of predators and parasit• oids was evident in California, accounting for the severity of the losses being incurred. An Australian correspondent, Frazer Crawford, had apprised him of at least one parasitoid, a dipteran, Cryptochaetum iceryae (Williston), which de• stroyed the scale, and Riley suggested that the State, or even the County of Los Angeles, support the mission of an expert entomologist to Australia for the pur• pose of studying, collecting, and shipping beneficial insects back to California. Because of politico-budgetary problems in Washington, Riley was temporarily prevented from sending his own representative on the mission. However, in Au• gust, 1888, Albert Koebele set sail for Australia, ostensibly as a representative of the United States Department of State at an International Exposition in Mel• bourne, but in reality to collect insect enemies of I cerya as Riley's agent. Previous to Koebele's departure, W. G. Klee, California State Inspector of Fruit Pests, had independently received and liberated some Cryptochaetum flies from Crawford in Australia. It was not until Coquillett introduced beneficial insects from Koebele, under Riley's direction, that things really began to happen. Although Riley originally had more confidence in the potential of Cryptochae• tum, it soon became apparent to all concerned that a small lady beetle discovered feeding on Icerya by Koebele was the solution everyone sought. Small numbers (129 individuals) of the vedalia beetle, R. cardinalis (Mulsant) (Fig. 1), were initially received between November, 1888, and January, 1889, and were used as breeding 24 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

Fig. I. The vedalia beetle, Rodolia cardinalis (M ulsant), a coccinellid predator of the cottony• cushion scale, [cerya purchasi Maskell, and a classical example of an agent of biological insect pest suppression stock. By June, 1889, over 10000 offspring of these first imports had been pro• duced and distributed to hundreds of orchards in southern California. Two later shipments of beetles, a total of 385 specimens, arrived in February and March and were immediately released. In nearly every case of colonization an almost phe• nomenal decrease in I cerya infestation occurred within scant months. By the following season cottonycushion scale had nearly disappeared and was no longer a problem of significance. The citrus industry was saved, and the vedalia was acclaimed as a miracle of applied entomology. The cost of the project was as• sessed at about $ 1500.00 (Doutt, 1964). A secondary benefit of the importations was that Cryptochaetum also became established and is today an important scale enemy in coastal areas around San Fransisco and in some parts of southern California. Koebele became a local hero, and in his native Germany, the practice of biological pest control was known for some time as the "Koebele method." Oth• ers have an equal or greater claim to responsibility for the successful program, notably Riley, but the important fact is that biological control had come of age. The results of the project were well publicized around the world, and other countries with Icerya problems clamored for vedalia from California. Most every• where it was introduced, spectacular repeat performances occurred. In the wake of the vedalia experience, biological insect pest suppression went through a period of great popularity in many places, but especially in California. So many things were happening in various contexts that it would be impossible to cover them all, but we will follow a few developments and touch on certain significant projects in an effort to show where the philosophy was heading and how it got there. Impressed with Koebele's work, the California legislature appropriated $ 5000.00 in 1891 for further beneficial insect importations from Australia, and Middle History to 1940 25 prevailed upon Riley and the United States Department of Agriculture to cooper• ate financially by subsidizing Koebele as the man for the job. Koebele was gone for a year, during which time he sent back 46 species of Coccinellidae from Australia, New Zealand and Fiji, four of which became established. Only Crypto• laemus montrouzieri Mulsant, a mealybug predator, even approached the useful• ness of the vedalia beetle, however, Koebele eventually left California for a similar position in Hawaii in 1893 (Howard, 1930), where he aided in the introduction of a number of beneficial insects before finally returning to Germany in 1912 (Ord• ish,1967). The state of California employed a number of foreign collectors after Koebele, beginning with George Compere in 1899, and including H.L. Viereck, c.P. Clau• sen, and finally Harold Compere (son of George) in 1927-1928 (Essig, 1931), and has subsequently built one ofthe strongest facilities for biological control work in the world. Much of the early enthusiastic support for the method was sustained by the efforts of the chairman of the State Board of Horticulture, Ellwood Coop• er, who expressed himself in 1907 as follows (Essig, 1931):

California is to be congratulated upon the fact that she is the pioneer in the work of fighting insect pests with their own natural enemies. For years we have stood alone in this work, but our example is now being followed by very many states and territories and by foreign nations, and this state is looked to as the great exemplar in this work. It is true that the good work done by predacious and parasitic insects has been known for a great many years, but it remained for California to give a practical turn to this work, and introduce beneficial insects for work upon the destructive species. L. O. Howard, another early proponent of the use of beneficial insects, first suggested intercountry parasitoid transfer in 1880, and also took up the study of chalcid taxonomy in response to the absence of any progress in that area at the time. He described many new species and maintained a card file of host-parasitoid relationships on a worldwide basis. As Riley's successor as Chief of the Division of Entomology in Washington, Howard was a very influential man. Criticisms made by Howard of the development of biological pest suppression in California were bound to have more serious effects than if made by a lesser man, but nevertheless the method flourished for a time. In his autobiography, Howard (1933) com• mented that because of the vedalia success "it is safe to say that progress in the battle against injurious insects on the western coast of the United States was set back for ten years or more on account of the supreme reliance on this method of fighting pests and consequent abandoning of every other means and every other line of research." Howard also translated for English publication a paper by Marchal (1908) which was only slightly less critical of excessive confidence in biological control methods in California and Australia. Doutt (1964) strongly disclaimed Howard's criticisms, however, citing numerous examples of progress in methods other than biological control during the period. The running dispute between federal and state entomologists over the prosecution of biological pest suppression in California all but ended in 1912 with the appointment of H.S. Smith to head up the program. One of Howard's main criticisms of California's insect importation programs was the lack of competent, trained supervision, which he felt could only lead to careless movements of pest insects and introduction of such anathemas as hyper- 26 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression parasitoids. Smith was recognized in Washington as a capable trained entomolo• gist who was able to cooperate with federal officials, and thus the prospect of quarantine proceedings to stop importation of beneficial organisms into Cali• fornia was avoided by his appointment. The confidence extended to Smith was well deserved, for his accomplishments were many and significant (Hagen and Franz, 1973). His responsibilities for importation and screening of natural ene• mies were first at the state insectary, later at the University of California Citrus Experiment Station, and finally under the statewide Department of Biological Control of the university. He organized and constructed new laboratories and facilities, aiding in the early development of biological weed control with C. B. Huffaker and J. K. Holloway, and an insect pathology laboratory under E. A. Steinhaus. Smith (1919) was even the first to propose the term "biological con• trol," and wrote voluminously (1935, 1939) on the theoretical aspects of the study. During the closing years of the nineteenth century, when most of the entomo• logical world was captivated by the idea of controlling pests with introduced parasitoids and predators, a few workers were still pursuing the study and use of insect pathogens (Steinhaus, 1956). A number of European scientists, stimulated by MetchnikoWs recommendations, advocated and used various fungal patho• gens with variable success. Entomophthoraceous fungi were suggested for fly larvae, grasshoppers, and other insects, and Beauveria spp. were tried against nun moth caterpillars, Porthetria monacha (L.), and Melolontha beetles. It soon be• came apparent that success was greatly dependent upon an adequate supply of environmental moisture and sufficient knowledge of how to use the fungi properly to cause epizootics at will. In the midwestern United States, a large and well• publicized project was undertaken to control the chinch bug, Blissus leucopterus (Say), with a fungus, Beauveria globulifera (Spegazzini) Picard (= B. bassiana (Bal• sarno) Vuillemin). Two prominent entomologists of the time, F. H. Snow in Kan• sas and S.A. Forbes (e.g. 1895) in Illinois, were most responsible for administering the distribution of thousands of packages of fungal spores free of charge to farmers for field introduction. Other states had similar programs, but in all cases the results were ambiguous enough to cause their abandonment. Artificial dissem• ination of the fungus did not seem to appreciably increase the natural occurrence and effectiveness of the disease. However, the project did publicize the idea that microbial pathogens, like parasitoids and predators, had a potential for the sup• pression of noxious insect pests. According to Steinhaus (1956), the year 1900 was the approximate peak date of excitement for early workers dealing with insect diseases, and this enthusiasm and effort persisted for over 30 years before subsid• ing temporarily into skepticism and discouragement. California was not the only place where significant development of biological control was occurring. For example, in 1893, Albert Koebele was hired by the Hawaiian government to continue there the work he had done in California. Koebele's vedalia had previously been introduced to Hawaii with great success. An invasion of Hawaiian sugarcane fields in 1900 by an Australian leafhopper, Perkinsiella saccharacida Kirkaldy, caused the organization of a Division of Ento• mology by the Hawaiian Sugar Planters Association (Timberlake, 1927). R. E. L. Perkins was in charge and Koebele was one of several other staff members. This industrious group of workers was responsible for a large number of successful Middle History to 1940 27 biological control programs with the result that the early history of economic entomology in Hawaii is almost synonymous with their work. The leafhopper pest problem was eventually completely suppressed after a series of beneficial insect introductions beginning with egg parasitoids from Australia and culminat• ing in 1920 with the predaceous mirid, Cyrtorhinus mundulus (Breddin), which completed the job. The principles and experience accumulated in this and other successful programs conducted in Hawaii by the Sugar Planters Association and the government have all contributed to the development of the practice of biologi• cal insect pest suppression. In Italy, during the early 1900s, biological control activities were advanced by two outstanding entomologists, A. Berlese and F. Silvestri (Howard, 1930). Their efforts might have been more productive had not a serious difference of opinion and subsequent arguments developed between them in regard to the advisability of introducing one or many species of beneficial insects, and the superiority of parasitoids or predators. Berlese was responsible for initiating a very successful biological control program in 1906 when he imported a parasitic wasp, Prospal• tella berlesei (Howard), from L. O. Howard in the United States for control of a troublesome scale insect, Pseudaulacaspis pentagona (Targioni-Tozetti), on mul• berry. Like the vedalia, this parasitoid later was used successfully against its host in several other countries around the world (DeBach, 1964 b). Several other important early attempts at biological pest suppression oc• curred in the United States under the auspices ofthe United States Department of Agriculture. One of the largest of these was the gypsy moth campaign which served to develop basic ecological principles, brought to light much new biologi• cal and taxonomic information regarding entomophagous insects, and, most im• portantly, influenced a group of scientific investigators who became leaders and teachers (Hagen and Franz, 1973). The importation of beneficial insects from Japan and Europe against the gypsy moth, Porthetria dispar (L.), took place from 1905 to 1914, and again in 1922-1923. Nine parasitoids and two predators of the 40 species released became established (Clausen, 1956). Howard and Fiske (1911) were the chief administrators of the project, and A. F. Burgess, H. S. Smith, P. H. Timberlake, C.H.T. Townsend, and W.R. Thompson, all contributed greatly to this work and afterwards to the field of biological insect pest suppression in general. The effects of the gypsy moth program were felt strongly in Canada as well (Baird, 1956). A collateral interest in the United States program was the browntail moth, N ygmia phaeorrhoea (Donovan), which moved from New England into eastern Canada in 1909-1911. Cooperation between L. O. Howard and C. G. Hewitt, the Dominion Entomologist, provided immediate aid and equipment to collect and rear parasitoids and predators of the moth for introduction to Can• ada. Other important Canadian entomologists involved were: L. S. McLaine, J. D. Tothill, G. E. Sanders, A. B. Baird, and F. M. McKenzie. The first modest biologi• cal control laboratory in Canada was soon erected on the campus of the Univer• sity of New Brunswick, and by 1916 when importations ceased, three important parasitoids had been established, putting the method on sound footing for future development. Another massive program of beneficial insect importation was begun by the USDA in 1919, shortly after the European corn borer, Ostrinia nubilalis (Hiibner), 28 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

was first discovered in Massachusetts (Baker et al., 1949). A laboratory manned by H.L. Parker and W.R. Thompson was set up in France, and by 1940, 23 million larvae had been sent back for parasitoid rearing; another 3 million larvae came from Japan between 1927 and 1936. Six of the 24 species of parasitoids imported became established, but control was only partially obtained. In 1923 the Canadians again enlisted the cooperation ofthe USDA Bureau of Entomology to aid in their own corn borer suppression program carried out by Baird (1956). The biological control laboratory in Fredericton, New Brunswick, had ended opera• tions in 1922 and the new project was located first in St. Thomas, Ontario, and later in Chatham, where several additional projects were gradually added. Other important introduction programs carried on by the USDA in the 1920s and 1930s concerned the alfalfa weevil, Hypera postica (Gyllenhal) (Chamberlin, 1924), the Japanese beetle, Popillia japonica Newman (Clausen, 1956), and the European earwig, Forficula auricularia L. (Clausen, 1956), indicating a continued interest in biological pest suppression. In 1934, a Division of Foreign Parasite Introduction was organized, and it remained active in foreign investigations and quarantine handling of imported natural enemies until the increased use of pesti• cides in the mid-1940s caused its decline (Hagen and Franz, 1973). In 1927, the British Imperial Bureau of Entomology organized the Farnham House Laboratory for the purpose offurthering the study and practice of biologi• cal insect pest suppression in the countries of the British Empire (Baird, 1956). A conference of Canadian entomologists in Ottawa in that same year was attended by Howard and other influential American workers, and sowed the seeds for the planning of a central facility for biological control in Canada. By 1929, the facility, organized from the staff and equipment at Chatham, had been established at Belleville as the Dominion Parasite Laboratory. The staff, facilities and programs expanded rapidly, and by 1933 a new era in biological control was dawning in Canada. An all out effort, directed by 1. M. Swaine, was made against a severe infestation of the European spruce sawfly, Diprion hercyniae (Hartig), in eastern North America. The program was conducted in cooperation with the United States Bureau of Entomology and Farnham House Laboratory, and was immi• nently successful, as the introduced parasitoids and a fortuitously introduced virus disease soon checked the pest problem. In 1940, because of World War II, the Farnham House Laboratory was closed, and its Superintendent, W.R. Thompson, and staff, were housed at Belleville. Thompson's service group was later reorganized as the Commonwealth Institute of Biological Control (Baird, 1956). The preceding account might well suggest that only the large rich countries of the world were responsible for the advance of biological insect suppression. It is true that California, Hawaii, the United States Department of Agriculture, and Canada were leaders in the great expansion of the field between the introduction of the vedalia beetle and the beginning of World War II, but many smaller countries made significant contributions to the acceptance of the method as a useful viable practice worldwide. Among the group of countries most active in biological control, Fiji may be cited, particularly for its consistently well-orga• nized successful programs carried on by highly qualified entomologists. Between 1925 and the mid-1930s the ravages of a series of coconut pests were suppressed Middle History 1940 to 1962 29 through the efforts ofJ. D. Tothill, R. W. Paine, and T.H.C. Taylor, who imported their parasitoids and predators (Tothill et al., 1930; Taylor, 1935, 1937). And so the period of entomological history from 1888 to 1940 was a time of the sudden striking realization of the value of the technique of biological insect pest suppression; of its repeated demonstration in many parts of the world; of enthusiasm and the rapid expansion of a new discipline; and of great cooperation between entomologists and the countries they represented in getting the job done. There was, as yet, no suggestion of the poison that was soon to all but end the progress that had gone before.

2.1.3 Middle History 1940 to 1962

In 1874, a German chemistry student, Othmar Zeidler, synthesized a new organic chemical that was destined to have profound effects on the practice of biological insect pest suppression, and, for that matter, on human society in general. It was not until its rediscovery in the autumn of 1939 that this compound began its rise from relative obscurity to become one of the most famous (or infamous) and controversial agricultural chemicals in the world. Dr. Paul MUller, working in the Basel laboratories of the J. R. Geigy chemical company in Switzerland, discovered at that time the remarkable insecticidal properties of the compound which we now know as DDT (West and Campbell, 1952). The new insecticide found use in suppressing an outbreak of the Colorado potato beetle, Leptinotarsa decemlineata (Say), in Switzerland, but it was not intro• duced into the United States or Great Britain until 1942 when Geigy called the attention of the respective governments to its insecticidal properties. The USDA had been searching for a substitute for pyrethrum and derris insecticides made insufficiently available by the effects of World War II, and tests made in late 1942 against a number of leaf-feeding insects and body lice indicated great promise for DDT. An interesting analysis of research papers published by USDA scientists sheds useful light on the resulting problems of biological control work (Sailer, 1972). In 1915, the ratio of biological control research publications to insecticide research publications was 1: 1. This slipped to 0.3: 1 in 1925, and during the war years insecticide papers predominated 6: 1. The trend to insecticidal research and insect control was there earlier, but the advent of DDT was nearly a mortal blow. By 1946 the ratio had reached 20: 1. DDT and other subsequently discovered persistent organic insecticides came into wide use during this period, and because they were so spectacular and successful in their effects, little attention was given to biological control methods. Many felt that the approach was no longer valid, and that, in fact, no more than a passing knowledge of pest habits and biology was necessary to reduce popula• tions with toxic chemical applications. At the beginning of World War II the USDA employed about 40 entomologists full time in biological control research, but by 1954 the equivalent of only five were devoted to these problems (Sailer, 1972). 30 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

Thus it was that the focus in insect pest suppression strategy from the 1940s into the 1960s was on the use of chemicals; however, a few programs of interest and importance were carried on utilizing biological methods, indicating that faith in the practice was not entirely lost to everyone. European and Soviet efforts during these years were reviewed by Franz (1961 b) under three headings: microbial control, entomophagous insects, and entomophagous birds. Viruses, protozoa, bacteria, and fungi all found some suc• cess in limiting depredations by various insect pests. Of particular note was the resumption of interest in the use of the bacterium, Bacillus thuringiensis Berliner, which occurred simultaneously in Europe and America during the early 1950s. These studies resulted in a significant breakthrough when B. thuringiensis was first commercially produced in the late 1950s (Hall, 1964). Also significant was the growing emphasis on combining the use of microorganisms with other forms of pest suppression (i.e. chemical, physical, or cultural means) for greater effective• ness. Europe, as a whole, appears to have fewer introduced pest insects than other continents (Franz, 1961 b), and therefore was more active in exporting beneficial insects than in their importation. However, a number of parasitoids and preda• tors were successfully introduced, particularly in southern Russia, against pests of peach and citrus. European workers also increased their expertise in the utiliza• tion and encouragement of native beneficial organisms through environmental manipulation, a concept they widely accepted and strongly propounded. Methods such as safe integration of chemical applications with the life cycles of beneficial organisms, transfer of invertebrate predators, such as ants, within the continental area, and provision of nesting boxes for insectivorous birds, were all important accomplishments of these years. Another significant development was the estab• lishment of the International Commission of Biological Control in 1952 under the auspices of the International Union of Biological Sciences. The ICBC was re• cently reorganized as the International Organization for Biological Control (IOBC), but in its original form was composed of 22 members, including govern• ment agencies and official and private institutions from 16 countries of Central and Western Europe and the Mediterranean area. The group was designated to promote and coordinate national efforts in biological pest suppression by interna• tional cooperation within this geographical area of activity. The idea of the orga• nization was to compensate for a lack of expertise or facilities in each single country by a cooperative effort amongst all the member countries. All of the work undertaken was voluntary and there were no paid employees. The organization began publication of the journal, Entomophaga, and provided bibliographic doc• umentation and identification services for entomophagous insects, as well as providing one of the most positive signs of a resurgence of interest in biological methods of pest suppression in Europe at this time. Meanwhile in Canada, F. T. Bird carried out his excellent studies of the acci• dentally introduced polyhedral virus disease of the European spruce sawfly, D.hercyniae, and this encouraged the beginnings of a strong program of applied insect pathology in Canada (Cameron, 1956). By 1950, there was a well-equipped Insect Pathology Laboratory in Sault Ste. Marie concerned with diseases of forest insects, and another research group working with those of agricultural pests in conjunction with the Dominion Parasite Laboratory at Belleville. Another impor- Middle History 1940 to 1962 31 tant Canadian advance was the discovery by Wilkes (1942) that the principles of genetics could be applied to mass production of parasitoids for improving the qualities offecundity, vigor, longevity, or adaptation to the climate or habitat into which they would be released. A significant number of other biological control projects were undertaken in Canada during the 1940s and 1950s with varying success (McLeod et al., 1962), and by 1955 the Belleville laboratory, headed by A. Wilkes, had become one of the largest centers for such research in the world, taking on the name of Entomology Research Institute for Biological Control. Most of the projects concerned the liberation of imported insect parasitoids against pests which were usually also of foreign origin, and the Institute staff was invariably involved in each. The Commonwealth Institute of Biological Control (formerly Farnham House Laboratory) was headquartered at Belleville from 1940 to 1946 and at Ottawa from 1946 to 1961, and carried out the contractual respon• sibility for most of the overseas work required for the introductions. W.R. Thompson, Director of CIBC, was succeeded on his retirement in 1958 by F.J. Simmonds, and in 1961 the headquarters of the organization was moved to the present location in Trinidad, West Indies. Interest in biological insect pest suppression in the United States during the 1940s and 1950s was kept alive mostly in California, Hawaii, and in the United States Department of Agriculture. H.S. Smith remained in charge of the investiga• tions in California until C. P. Clausen succeded him in 1951. During the years of Smith and Clausen, mass-culture techniques were developed for both hosts and natural enemies, the insect pathology laboratory was formed, and successful at• tacks were mounted against a number of coccid pests, aphids, and spider mites, in addition to control of Klamath weed (Hagen and Franz, 1973). One of the largest biological pest suppression efforts ever organized took place in Hawaii during the late 1940s against the Oriental fruit fly, Dacus dorsalis (see 2.3.3.2), and the cooperation amongst entomologists of the half-dozen agencies involved was most encouraging, especially when substantial success was finally achieved. Though manpower for the purpose was much reduced, the USDA also had substantial success with biological suppression of a number of insect pests including: the citrus blackfly (1948-1957), the spotted alfalfa aphid (1955-1957), the eastern outbreak ofthe alfalfa weevil (1957-present), and the Rhodesgrass scale (1959). In 1959, a growing interest in insect diseases gave impetus to the publication of the Journal of Insect Pathology in New York (now Journal of Invertebrate Pathology). Aside from the few enumerated centers of activity which provided a reservoir of research in biological insect suppression and several progressive and innovative ideas, there was little of a positive nature to commend this period in history. And yet, a little more than a decade after the use of persistent organic insecticides became widespread, several unforeseen, insidious, and negative side-effects of that use were becoming apparent (Ripper, 1956). Although ill-informed blind applica• tions of toxic chemicals easily decimated pest populations, they also served as a strong selective force. No insecticide is 100% effective, and a few pest insects survived each application to produce another generation of offspring, each receiv• ing genetically the decreased susceptibility from its parents. Thus, resistance to the once all-powerful chemicals developed. For example, until 1949 cotton insects were suppressed with arsenicals or nicotine sulphate in the Canete Valley in Peru 32 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

(Smith and van den Bosch, 1967). The average annual yield of cotton per hectare was 526 kg until an outbreak of aphids and bollworm occurred in 1949, decreas• ing the yield to 365 kg/ha. Farmers began using chlorinated hydrocarbons, reduc• ing pest populations to low levels but also destroying beneficial insects. Cotton yields initially almost doubled, but one by one the new pesticides became ineffec• tive as resistance to them developed, and by 1956 the growing of cotton was economically impossible. Another side-effect pointed out by this example is the wholesale destruction of beneficial insects by broad-spectrum insecticides. In many other documented cases, such destruction has allowed previously unimpor• tant potential pests to become serious problems when the natural factors keeping their populations low are suddenly removed (pest "upsets"). Most of the new organic pesticides were persistent, a useful characteristic for ease in insect control. But the chemicals remained in the environment for long periods after their usefulness was ended, concentrating in plants and animals living there, and entering the food web of wildlife and man. Other problems, in addition to persistence and biomagnification soon became apparent, including acute toxicity to non-target organisms such as birds, fish, and wildlife, and poten• tial chronically produced problems of carcinogenesis, teratogenesis, or mutagene• SlS. One by one these various problems with organic pesticides came to the atten• tion of the scientific community and were discussed and debated among agricul• turalists, industrial producers, entomologists, and governmental officials. But not until 1962, with the publication of Rachel Carson's Silent Spring, did the debates take on urgent and epic proportions and come before the eye of the general public.

2.1.4 Recent History (1962) to the Present

It is very difficult to estimate the true impact of Silent Spring on the practice of pest management, but one thing is evident in retrospect. It eventually caused members of widely diverse segments of the world's population to think about and discuss (albeit many times from a less than knowledgeable viewpoint) something they had previously taken for granted or ignored~insect pest suppression. Ento• mologists and others directly involved had been aware of and concerned about the developing problems with synthetic insecticides for nearly a decade, and had already begun to seek alternative methods of control and to strengthen research on parasitoids, predators, and pathogens. But the newly acquired awareness and environmental concern of the general public called for accelerated and increased investigation into safer ways of protecting the health, food, and fiber of the world's people. Biological insect pest suppression was, and still is, one of the most promising areas in which to center our search. All of a sudden, except for a few hard core chemical control advocates, every• one became at least a "lip-service" ecologist. Research specialists and pest control operators, home gardeners and corporate farmers, began to at least think before applying chemical pesticides. The environmental impact statement was born. Recent History (1962) to the Present 33

Entomologists sought to find any connection, no matter how tenuous, between their research studies and alternative methods of pest suppression. And those who had maintained their faith and interest in biological pest suppression looked on in wonder, with perhaps a tinge of bitter satisfaction, as more and more people began to see what had been so clear to them all along. A number of thoughtful books have appeared recently which further examine the place of agricultural chemicals in today's world (Rudd, 1964; Graham, 1970; SWIft, 1971; Whorton, 1974), and/or discuss the relation of pesticides to the many• faceted array of alternatives which are being developed (President's Science Advi• sory Committee, 1965; National Academy of Sciences, 1969a, 1972). Several re• cent localized and broad range historical treatments of biological control have also appeared (Johansen, 1957; Commonwealth Institute of Biological Control, 1971; Greathead, 1971; Rao, 1971; Rao et aI., 1971; Sailer, 1972; Hagen and Franz, 1973; Mertins and Coppel, 1974). All of these, and others, indicate the tremendous interest currently afforded the theories and practice of biological pest suppreSSIOn. The two multinational cooperative groups organized to promote the cause of biological control are today stronger than ever. F.J. Simmonds presides over the Commonwealth Institute of Biological Control from its headquarters in Trinidad, West Indies. More than half a dozen field stations are maintained around the world to provide collection and rearing services for beneficial organisms. The Institute is basically maintained by contributions from member nations of the British Commonwealth, but does contract work for other nations as well. The actual costs of each project undertaken must be fully covered by the country seeking the services of CIBC. The International Organization for Biological Con• trol was reorganized in 1971 and has now expanded beyond the original 16 countries of Europe and the Mediterranean area to include individual and organi• zation members from nearly all the major countries of the world. There are currently three regional sections with two more being organized as follows: the West Palearctic Regional Section including the original ICBC countries, the Western Hemisphere Regional Section, the South and East Asian Regional Sec• tion, the Tropical Africa Regional Section, and the Pacific Regional Section. IOBC remains as the important conduit for the exchange of ideas and informa• tion regarding biological control on a worldwide basis. Under the broad definition of biological insect pest suppression adopted by this book, that is, the use of any organism or its products to the detriment of the pest insect, many new, unique, and forward-looking techniques may be consid• ered. And we will do so in subsequent chapters, leaving the discussion of the major developments in the field during recent times to make up the bulk of what follows. The realization ofthe necessity for more biological and ecological studies of the pest insect and its present and potential natural enemies has lead to a number of new concepts, such as the life table, population models, systems analy• sis, and the agroecosystem concept. These, in turn, have given rise to such terms as supervised pest control, bioenvironmental control, integrated control, and pest management systems. The components and tools in use and under study include parasitoids, predators, and pathogens, in addition to pheromones, attractants and hormones, host resistance and cultural practices, genetics and sterilization, natu- 34 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression ral and more selective insecticides. All of these things have their place in current insect pest suppression practices and will be discussed hereinafter. For now, let us conclude this history of the development of biological insect pest suppression by saying that the mood of the concerned scientific community is now such that great progress is within reach. Greater and more diverse research effort is being expended than ever before in hitherto undreamed of fields. Biologi• cally sound solutions to pest problems on a very narrow scale, or with extremely broad application, are surfacing with more frequency every month, and if as much money and effort were applied to the search for these solutions as is expended on the development of chemical insecticides, historical reviews such as this would become obsolete before they could be published.

2.2 Dynamics of Natural Populations as a Basis for Biological Insect Pest Suppression

It does not require a great deal of research or experience to discover an important characteristic of insect population phenomena. That is, some species consistently occur in large numbers (i.e. are common) while others are comparatively rare. Observe, for example, the butterflies flitting amongst the flowers in any suburban area of grassy fields, gardens, and scattered woods. During midsummer in the midwestern United States such a scene would be alive with the medium sized clouded sulphur butterfly, Colias philodice Latreille; an occasional large orange and black monarch butterfly, Danaus plexippus (L.), would drift by, but it would be not at all common to observe the large black swallowtail, Papilio polyxenes asterias Stoll. These relative population densities are maintained year after year. The absolute numbers of one or all of the species may vary from time to time, but in general the Colias is most abundant, the Danaus much less numerous, and the Papilio, comparatively rare. What causes these differences in relative population size? And for that matter, why do the absolute numbers vary with time? Are the particular observed population densities intrinsically characteristic of each spe• cies, or are they the effect of some extrinsic factor or factors? These and other questions have fascinated and troubled ecologists and entomologists for a long, long time, and have generated a voluminous amount of literature and some heated debates and discussions amongst those workers who have attempted to answer them.

2.2.1 The Ground Rules

The study of the dynamics of natural populations has a long history, and the methods used are mostly observational and theoretical. Interestingly enough, some of the earliest important writings on the subject were those of an economist discussing moral philosophy and the theory of human history. Thomas Malthus (1798) was probably the first to inquire into the means by which population levels are maintained, and in doing so became world-renowned for the so-caned Mal- The Ground Rules 35 thusian Theory. He concluded that "population, when unchecked, increases in a geometrical ratio. Subsistence increases only in an arithmetical ratio. . .. This implies a strong and constantly operating check on population from the difficulty of subsistence .... The race of plants, and the race of animals shrink under this great restrictive law. '" Necessity, that imperious all pervading law of nature, restrains them within the prescribed bounds ... it's effects are waste of seeds, sickness, and premature death. Among mankind, misery and vice." Although Malthus directed his discussion toward the ultimate fate of humani• ty, he did not fail to draw some parallels to the factors limiting plant and animal populations. By 1859 the ideas of Malthus were well-known, and to Charles Darwin they comprised one of the major considerations in the development of his thoughts On the Origin ojSpecies: Every being, which during its natural lifetime produces several eggs or seeds. must suffer destruction during some period of its life. and during some season or occasional year, other• wise, on the principle of geometrical increase. its numbers would quickly become so inordi• nately great that no country could support the product. Hence, as more individuals are produced than can possibly survive, there must in every case be a struggle for existence. either one individual with another of the same species, or with individuals of distinct species, or with the physical conditions of life. It is the doctrine of Malthus applied with manifold force to the whole animal and vegetable kingdoms: for in this case there can be no artificial increase of food, and no prudential restraint of marriage .... There is no exception to the rule that every organic being naturally increases at so high a rate, that, if not destroyed, the earth would soon be covered by the progeny of a single pair. ... In looking at Nature, it is most necessary to keep the foregoing considerations always in mind-never to forget that every single organic being may be said to be striving to the utmost to increase in numbers; that each lives by a struggle at some period of its life; that heavy destruction inevitably falls either on the young or old, during each generation or at recurrent intervals. Lighten any check, mitigate the destruction ever so little, and the number of the species will almost instantaneously increase to any amount. In discussing the nature of the checks to theoretical geometric increase, Dar• win commented further: The causes which check the natural tendency of each species to increase are most obscure . ... The amount of food for each species of course gives the extreme limit to which each can increase; but very frequently it is not the obtaining food, but the serving as prey to other animals, which determines the average numbers of a species .... Climate plays an important part in determining the average number of species. and periodical seasons of extreme cold or drought seem to be the most effective of all checks .... The action of climate seems at first sight to be quite independent of the struggle for existence; but in so far as climate chiefly acts in reducing food, it brings on the most severe struggle between individuals. whether of the same or of distinct species, which subsist on the same kind of food. Even when climate, for instance, extreme cold, acts directly, it will be the least vigorous individuals, or those which have least food through the advancing winter, which suffer most. ... When a species, owing to highly favorable circumstances, increases inordinately in numbers in a small tract, epidemics ... often ensue; and here we have a limiting check independent of the struggle for life .... The dependency of one organic being on another. as of a parasite on its prey, lies generally between beings remote in the scale of nature. This is likewise sometimes the case with those which may be strictly said to struggle with each other for existence, as in the case of locusts and grass-feeding quadrupeds. But the struggle will almost invariably be most severe between individuals of the same species. for they frequent the same districts, require the same food. and are exposed to the same dangers .... In the case of every species, many different checks, acting at different periods of life. and during different seasons and years. probably come into play; some one check or some few being generally the most potent; but all will concur in determining the average number ur evenlhe existencc of the species. 36 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

Darwin was not so much concerned with the control of the absolute size of the animal populations caused by competition and the "struggle for existence" as he was with another result of this struggle, "natural selection or the survival of the fittest." Nevertheless, he presented a lucid enumeration and discussion of the various processes which determine population densities, and in doing so was one of the first biologists to deal with the relative importance of competition, preda• tion, and climatic factors in this regard. As we have seen in Chapter 2.1, there was some inkling of the importance of certain factors in the gross mortality of pests as early as the 1700s by Rcaumur and Linnaeus. Others, notably Kollar, Fitch, and Walsh, emphasized particular mortality factors during the 1800s, and Darwin dealt with a number of ways in which he felt populations were kept in check; but it was not until the report of Howard and Fiske (1911) on the gypsy moth that a clear-cut mechanism was proposed for the function of the various factors in insect population regulation. In the 65 years since that time, the basic ideas presented by Howard and Fiske have been accepted, rejected, discussed, and elaborated to a voluminous extent. Studies of population regulation processes in many animals and plants have been carried out, but probably no more important contributions were made than those of entomologists, and in particular biological control spe• cialists.

2.2.2 "Natural Control": The Ecological Basis for Biological Insect Pest Suppression

We observed earlier the relative stability of average population densities of three species of butterflies; one common, a second less common, and the third compar• atively rare. In a stable environment (i.e. one not undergoing a catastrophic disturbance by man or the elements), such stability in abundance is an easily observable characteristic of all living organisms. And yet, observed from a differ• ent perspective, population density is never static; in fact, it is always fluid and changing. Thus, throughout the year, individuals which make up the population are dying of senescence, starvation, predation, exposure or accidents; reproduc• tion occurs, and new individuals come into the population; immigration and emigration also take place. Populations can, it seems, be both stable and changing in numbers at the same time. In visualizing this phenomenon an analogy to the sea is frequently employed with success (Smith, 1935; Doutt, 1972). It is univer• sally accepted that sea level is a constant from which altitudes are to be measured, and, yet, how rare is the time and place where the surface of the ocean is perfectly flat and motionless! Sea level is the long term average in time and space about which the surface of the waters ceaselessly moves. Similarly, we observe that although the population density of an organism may be constantly changing, the value tends to oscillate about a mean which is comparatively stable, although also subject to change under certain conditions. The preceding statement combines the major components in the concept of natural control, which is defined as the maintenance of this dynamic equilibrium within particular upper and lower limits over a period of time by a complex combination of all the environmental factors impinging upon the population. The Processes Responsible for Modifying the Size of Insect Populations 37 resiliency of the population in returning to the characteristic mean density after periods of positive or negative excess is most important. Although at first glance the tendency seems remarkable, its necessity is soon evident in light of the pro• jected dire consequences to the species of continued increase or decrease in num• bers. This is the so-called "balance of nature" enunciated since the time of Lin• naeus. The balance of nature is the result of natural regulative processes in the environment of every living thing, and it assures that a species will neither decline in numbers to extinction nor increase to infinite density. Referring back to the three butterfly populations, we observe that regardless of whether a species is abundant or scarce, the average characteristic density of its population in a given habitat is constant. Note that in other habitats the density may be higher or lower, or if certain conditions are changed in the given habitat the density may be affected as well, but in an undisturbed environment long-term population stabil• ity is a truism. The importance of this ecological principle should be self-evident, for without it the living natural world would cease to exist.

2.2.3 Processes Responsible for Modifying the Size of Insect Populations

The study of numerical changes occurring in populations is variously known as population dynamics, demology, or larithmics, and is really nothing more than quantitative population ecology. Population dynamics is concerned not only with observing and describing how the population size of a species varies in time and space, but also with separating out and understanding the processes which cause the variation. The first ecologists were primarily concerned with studies of aute• cology and the influence of the environment on individual organisms. Gradually, as the factual and conceptual bases of ecology became more sophisticated and biometrical techniques were adopted, the emphasis shifted to synecology and quantitative popUlation ecology. A number of early workers in the field had a primary interest in the mathematical description of population size variation (Pearl and Reed, 1920; Thompson, 1922a, b, c, 1924; Lotka, 1925; Pearl, 1925; Volterra, 1926; Chapman, 1931; Gause, 1934, 1935), and to them we owe credit for theoretical and practical demonstrations of such concepts as the logistic growth relationship of popUlations, biotic potential and environmental resistance, and descriptions of the interactions of two species predator-prey systems. Early ecologists noted that through appropriate sampling methods they could estimate the population density or the total number of individuals of an insect species in a given area at frequent intervals. Data such as these could be used to construct a graph representing variation in numbers with time. Such a graph is called a population curve. The shape of a population curve can be defined mathematically in terms of three variables: birthrate, death rate, and (in the case of a conveniently sized finite subpopulation) rate of movement into or out of the area (Clark et a!., 1967). The processes which influence the rate of change of each of these three variables are, therefore, also responsible for the observed changes in population density. 38 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

The processes responsible for causing variation in numbers of insects, humans, or other living things, are multifarious, and their interactions are complex. As we noted earlier, Malthus and Darwin were two early writers who enumerated sev• eral examples (i.e. war, delayed marriage, limited food supply, disease, competi• tion, etc.), and dozens more have been proposed over the years by others. Clark et al. (1967) recognize only two basic elements which influence the rate of change of the three variables: species characteristics and environmental influences. Each of the variables is affected differently by these interacting codeterminants. Thus, the birth rate of a population is determined primarily by innate characteristics of the subject species with only slight input from environmental considerations; disper• sal rates are determined by a more or less coequal interplay of species characteris• tics and environmental influences interacting upon individuals in the population and causing some to emigrate and some to stay; death rate is influenced most heavily by environmental processes with modification by species characteristics. Given these observations, and our concern with methods of biological insect pest suppression, it follows that the processes included in the totality of environmental influences are the most important to us here. With the exception of the sterile insect method of pest suppression (see Chap.4.3) whereby we can modify the reproductive rate of an insect population, it is difficult to imagine how we might change the species characteristics of a pest species to our benefit. There are some indications that this may be accomplished naturally, for example, when an in• crease in the population density alters the phenotypic or genetic character of an insect population so as to reduce its numbers (at least locally) in the next genera• tion (Pimentel, 1961, 1968; Hughes, 1963; Chitty, 1965; Klomp, 1966), or indi• rectly when an age selective mortality agent removes significant numbers of fe• males before they reproduce. However, for the most part, the determinants of insect population density potentially available to us for direct beneficial modifica• tion are included in the environmental processes, and particularly those which influence the death rate. Howard and Fiske (1911) were the first to propose a systematic mechanism encompassing all the mortality factors, as they perceived them, which would account for insect population regulation. In their classic study of the gypsy moth and the browntail moth, N.phaeorrhoea (Donovan), Howard and Fiske recog• nized three kinds of mortality processes: (1) facultative agencies which destroy a larger proportion of the population as abundance increases, (2) catastrophic agencies which are totally independent of rarity or abundance in their effects, and (3) agencies, including birds and other predators, which act in a manner opposite to the facultative agencies, destroying a certain gross number of individuals each year, regardless of abundance, as a part of their diversified diet. Terms proposed by Smith (1935) for the ideas first expressed by Howard and Fiske have now become widely accepted as more graphically descriptive of the processes. Thus, facultative agencies are called density-dependent and catastrophic agencies are density-independent. The third category is now usually referred to as inversely density-dependent, and such agencies are generally regarded as having little im• pact on the determination of average population density (Smith, 1935). The school of early mathematically oriented population dynamicists including Pearl and his successors was followed and complemented by another group of Processes Responsible for Modifying the Size of Insect Populations 39 ecologists, many of them entomologists, who attempted to clarify, improve, and extend the proposed theories and mathematical models through studies of natural populations (Thompson, 1930, 1939; Uvarov, 1931; Nicholson, 1933, 1954, 1958; Nicholson and Bailey, 1935; Smith, 1935, 1939; Solomon, 1949, 1957; Andrewar• tha and Birch, 1954; Milne, 1957). The investigations and writings of these and many other population ecologists led to lively, and at times, heated debates about relative importance of the various regulating mechanisms involved in the determi• nation of the abundance of living things. The crux of the controversy was whether population levels are controlled by density-independent processes, such as cli• matic conditions, as proposed by Thompson, Uvarov, and Adrewartha and Birch; or by density-dependent processes, such as competition, parasitoids, pred• ators, and contagious diseases, as proposed by Malthus, Howard and Fiske, Nicholson, and Smith. In essence, of course, everyone was examining and evaluat• ing the same biological processes, and the theories and models they propounded were simply different ways of describing what was there for anyone to observe. Unfortunately, the observations were sometimes incomplete or inadequate, and the descriptions colored by personal preference and bias toward one's own inter• est and point of view. Problems in semantics and word definitions arose. Some authors placed emphasis on one aspect of the problem, some on another, some tried to take an overall view; and, of course, each individual frequently based his conclusions on observations of a different population system, some of which were probably more easily analyzed for a given aspect than another. The great diversity of theories no doubt reflects the exceedingly complex nature of the interacting processes they attempt to represent. Some are more useful and acceptable than others, but all are valuable for the constructive stimulation they provide. More recently a number of more or less extensive discussions of insect popula• tion dynamics have attempted to put the entire subject into perspective, especially in relation to pest suppression (Huffaker and Messenger, 1964 a, b; Clark et al., 1967; Southwood, 1968; National Academy of Sciences, 1969a; den Boer and Gradwell, 1971; Huffaker et al., 1971; McLaren, 1971; Bartlett and Hiorns, 1973; Varley et al., 1974). Two points seem to emerge from these discussions. First, as previously recognized, the complexity of the interacting processes responsible for the determination of insect numbers is still a pervading theme, but it is yielding to our understanding and the use of population models and computer analysis. Secondly, current thinking favors a comprehensive moderate viewpoint of the relative importance of various components in the population determination mechanism in nature. No one element is overemphasized and the situational importance of each receives recognition. These components of determination are still recognized as comprising two groups: the species characteristics, which we can do little to modify, and the environmental influences, some of which can be manipulated by man to the detriment of insect pests. The mortality factors in• cluded in the environmental influences remain divided for convenience into two groups: density-independent forces including primarily weather and climatic va• garies, and density-dependent forces which frequently result from the actions of parasitoids, predators, infectious desease, or competition for a finite supply of food or space. Here again we can see that at present there is little that we can do to suppress pest populations by modifying the physical (= abiotic) conditions of 40 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression weather or climate (however, see Chap.4.2 for potential methods of changing microclimate through environmental modification and Chap.4.l for the use of host resistance in the pest's environment). What remain of the elements responsi• ble for "the balance of nature" are the agents of density-dependent mortality. In this group of mostly biotic agents we most often find what we seek, natural control agents which we can manipulate to suppress pest populations. Before proceeding further with how we go about using biotic agents in pest suppression, let us briefly examine the current view of the natural control mech• anism. First of all, due to the great diversity of life in general, and insects in particular, no single general mathematical expression is available, even in com• puter language, which can adequately describe every population situation we may study. However, a generalized verbal understanding has evolved from the discus• sions and ideas put forth by the population ecologists mentioned in the preceding paragraphs. It recognizes all of the elements of natural control as important in their own right, depending on circumstance, and can serve as a guide in the study of any particular population. Reasonable discussions of the view are presented by Clark et aI. (1967) and Huffaker et aI. (1971), and these, in turn, are influenced most strongly by the ideas of Nicholson and Smith. The natural control mechanism, as currently formulated, is a composite pro• cess which at some point must include at least one element exhibiting density• dependence. Three broadly defined components are generally recognized as nec• essary elements in the interactions of a population and its environment. These are (1) the intrinsic characteristics of the population, (2) the so-called conditioning forces or influences of the environment, which, in a largely density-independent manner, set an interim framework of potential environmental capacity for the population, (3) a density-dependent governing or stabilizing mechanism, similar in operation to the idea of feedback in cybernetics, which regulates the population size in relation to the species characteristics and the existing environmental framework. The density-dependent regulating mechanism may in some cases be identified as one key factor which is largely responsible for determining popula• tion size (Huffaker, 1957; Morris 1959), or in other cases may be a collection of several factors operating at different times, but effecting the same overall stabiliza• tion of numbers (Huffaker et aI., 1971). If only one key factor is involved in the stabilizing mechanism, other density-dependent (but nonregulating) factors operating on the population might well be considered as interim components ofthe conditioning environmental framework (Clark et aI., 1967). It appears that most natural populations are subject to stabilization or regula• tion of numbers about some mean characteristic density by such a governing mechanism which operates most of the time. Thus, our three butterfly popula• tions each exhibit species characteristic additive properties of behavior, reproduc• tion, and migration which permit survival and increase in their numbers. For each species these additive processes are tempered and offset to a certain variable degree by the conditioning subtractive forces of their particular environment (e.g. adverse weather, limited availability of food or shelter). Finally, each species is subject to one or more regulating subtractive processes (e.g. parasitoids, predators or infectious diseases) which, operating in a density-related fashion, tend to re• duce the density of the population to its observed relatively stable characteristic Biological Insect Pest Suppression: Applied Quantitative Ecology 41 level. Other species populations, for example, locusts (Andrewartha and Birch, 1954), may persist for long periods of time at widely fluctuating densities which are apparently determined by extreme variability in some important environmen• tal characteristic (i.e. weather conditions, or indirectly their effect on available environmental resources). However, even these species are subject to eventual numerical regulation in relation to their variable environment by some density• related limitation (e.g. intraspecific competition and mass migration), although the density-dependent stabilizing processes which are present in the stable envi• ronment of populations of most species, and which operate at much lower densi• ties, may be absent.

2.2.4 Biological Insect Pest Suppression: Applied Quantitative Ecology

The vast majority of insects occur at population densities which exclude them from classification as pests. In fact, estimates presented by DeBach (1974), for example, indicate that only 1% of the insect species in North America could be classified as pests. Natural control processes suppress population densities of the other 99% to innocuous levels. Pest status originates in four ways (Clark et aI., 1967): (1) entry of a species into a previously uncolonized region, frequently through human agency; (2) evolutionary changes in the characteristics of a pre• viously innocuous species bringing it into conflict with humans; (3) changes in human activities which sensitize them to species previously regarded with indiffer• ence; (4) increased abundance of species whose interference with human activities was previously negligible because of their low population density. Such increases usually arise because of a protracted increase in the availability of a limiting resource, a lasting decrease in the effects of subtractive environmental processes which previously restrained the species from full realization of its potential for increase, or a combination of the two changes. With the relatively minor excep• tion of the evolutionary causes mentioned in (2), we can see that pest status generally originates from ecological changes involving the interrelations of hu• mans, the pest species, and the environment they share. To quote Clark et al. (1967):

It follows that the scope of pest control is limited essentially by man's ability to exploit potentially favorable ecological relationships. He cannot hope to avoid pest relationships, but he can strive to minimize their repercussions on his economy by manipulating the life systems of the species concerned. For purposes of control, pest situations are therefore best conceived as problems whose solutions should, ideally, stabilize the numbers of the life forms in• volved-at levels entailing the least possible disadvantages under the prevailing economic conditions. In other words, when ecological changes produce new pests, the logical human response should be a counteractive ecological manipulation aimed at perma• nently suppressing their numbers and/or economic effect. The philosophy of biological pest suppression rests on the belief that the density of many pest species is subject to reduction by ecological manipulation of suitable biological or environmental processes to make them less hospitable to 42 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression the pest. These manipulations may involve the species characteristics, the condi• tioning functions of the environment, or the density-dependent governing pro• cesses. In the case of the classical methods of biological control, the natural control theory we have just discussed is applied in practice by introducing (or encouraging the activities 01) agents of the density-dependent regulating process in the environment of the pest. Such agents are usually parasitoids, disease organ• isms, or various kinds of predators. If the proper selections are made, the density of the pest may be reduced permanently to levels at which it is no longer a pest. In terms of the theory of natural control, the characteristic average density or equi• librium position of the population is changed from one at which the activities of the pest insect interfere with human interests, to one at which these activities have negligible effect; this is accomplished by the addition of a natural enemy of the pest capable of acting in a density-dependent manner to regulate the population density about the new equilibrium position. Other methods of biological insect pest suppression may achieve their pur• pose through modification of other processes. For example, the species character• istic reproductive, behavioral, or developmental functions may be depressed through the use of genetic manipulation (Chap. 4.3), or hormones and phero• mones (Chap.4.4). Other environmental changes such as cultural manipulations (Chap. 4.2), or the introduction of competitors (4.3.3), or pest-resistant host material (Chap.4.1) may adversely modify the density-independent conditioning forces of the environment to such an extent that the potential carrying capacity of the environment, and hence the mean density of the pest population, is depressed. Our increasing knowledge and understanding of the mechanism of the dy• namics of populations, and development of the various methods of applying that knowledge for pest suppression are all very fine indeed. However, how are we to know which strategy to use for a particular pest in a given situation? The question of when a pest requires that suppressive measures be taken against it is comple• mentary to the question of which strategy is best. The answers to both questions, we believe, can be found in the imperative statement, know your insect. The application of our knowledge of quantitative ecology and population dynamics in the practices of biological insect pest suppression requires a more positive re• sponse to this statement than was ever needed for any of the expedient chemical methods of suppression. The necessity for more complete knowledge of the target insect in all its aspects is a recurrent theme of this book. A number of approaches have been adopted by entomologists to gain knowl• edge of insects. There are descriptive, observational, and experimental methods; there are taxonomic, morphological, histological, genetic, physiological, biologi• cal, ecological, behavioral, and biochemical studies. All of these approaches con• tribute to the basic library of knowledge upon which we may have to draw at any time to aid in the application of biological pest suppression. In regard to applied quantitative population ecology, perhaps the most important approach to data acquisition about insect pests is the development of life tables (Morris and Miller, 1954; Harcourt, 1969; Varley et aI., 1974). If population dynamics is concerned with studying the changing density of insect pests in time and space and under• standing the processes which cause those changes, then a life table is a device for expressing those observations in an orderly fashion, particularly in reference to Biological Insect Pest Suppression: Applied Quantitative Ecology 43 the age-specific distribution of mortality and its causes. Life tables were originally used in the study of human demographics, and most extensively by the life insur• ance industry which has an especial interest in age-specific survival rates (or, if you will, the inverse statistic, mortality rates). They have proved to be very useful in insect population dynamics, as well, especially with regard to univoltine insect species whose age-specific population parameters are much easier to sample than are those of multivoltine species. Development of a life table requires that the prevalence of all stages of the subject population, and all related mortality factors, be measured in terms of a common sampling unit. Samples may be taken over a period of several genera• tions in several different areas to generate separate life tables, or the resulting data may be pooled into a single life table. Selection and development of appropriate sound techniques for accumulating sampling data are most important, and equal emphasis should be placed on measuring the independent variables of weather, natural enemies, etc., along with the dependent variable, pest population density (Morris, 1955, 1960). When complete, the data are organized according to a number of conventions (Morris and Miller, 1954) into a life table (Table 1), which summarizes the initial density and survival rate within each stage of development, and the mortality factors present in each stage with their proportionate effects. If parasitoids or predators are important sources of mortality, useful interfacing life tables may be constructed for each ofthem also. A life table is a simple and efficient device for reducing a voluminous amount of data and presenting it in a readily analyzable form. Accumulation of the data reveals a number of immediately practical pieces of information such as emer• gence dates and duration of economically important stages, and perhaps a corre• lation between pest density and crop injury level (economic threshold), which may be used by growers for deciding on the necessity and timing of insecticide applica• tions or other suppressive measures. The economic threshold is a concept which allows us to decide when the population density of a pest is at a level requiring suppressive action to prevent economic damage. For example, feedback analysis of pest population sampling data, and its correlation with subsequent damage effects, may indicate that the presence of 10 or fewer pest insects in a given sample will result in a crop harvest reduction of an order below that which can be tolerated without significant economic loss (Beirne, 1967; Johansen, 1971). Thus, chemical preventative treatment may be omitted. Other definitions of economic threshold (Edwards and Heath, 1964) require that a decision be made as to whether potential damage will be less than or greater than the cost of preventative treatment. A consideration of how to define economic threshold is presented by Headley (1972), and Clark et al. (1967) discuss an important point frequently ignored in such determinations, the interrelations of a whole community of pests and their natural enemies to the economic damage caused by anyone of them. In terms of the theory of population dynamics, the aim of insect pest suppression is to maintain the equilibrium density of the pest population at a point below the economic threshold density in species that only occasionally exceed it in outbreak proportions. This type of situation is typical of forest insect pests whose numbers are generally stable at low densities for long periods between sudden, short-lived outbreaks. The emphasis here is on manipulating processes which cause or pre- 44 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

Table 1. Life table for 1967-1968 generation of the pine tussock moth, Dasychira plagiata (Walker)"

Age or stage (x) No. at beginning Morality factor No. dying Percent of of stage b (Ix) (dxF) (dx) stage dying (l00qx)

Eggs 215 Parasitoids 72.25 35 Infertility 17.20 8 Predation 8.60 4 Other 19.35 9 Total 120.40 56 Instar 1 94.60 Dispersion, etc. 9.46 10 Instar 2 85.14 Parasitoids 16.18 19 Fungi 19.58 23 Desiccation 3.40 4 Other 4.26 5 Total 43.42 51 Instar 2 41.72 Dispersion, etc. 15.44 37 Ins tars 3-{j 26.28 Parasitoids 17.08 65 Disease 0.79 3 Other 3.15 12 Total 21.02 80 Pupae 5.26 Parasitoids 2.68 51 Predation 0.26 5 Desiccation 0.16 3 Other 0.21 4 Total ----nT 63 Adults 1.95 Mortality 0.37 19 Reproducing Adults 1.58 Sex ratio, 0.5~ (i.e. Females x 2) Generation 213.42 99.26 Actual eggs 231 Expected eggs = 1.58/2 x 231 = 182.49 Population trend index = 18~i~9 x 100=84.88%, or a population decline of ca. 15%

" Modified after Sreenivasam et al. (1972). b Sampling unit: mean egg complement (fecundity) per individual female. vent outbreaks. In other species, more typical of agricultural environments, pest densities exist normally at equilibrium levels in excess of the economic threshold, either because of high pest populations, or a very low threshold making even scarce organisms into pests. Fluctuations in this instance are of little concern, and emphasis is on manipulating processes which determine the level of the mean characteristic density (National Academy of Sciences, 1969a). We can derive many other benefits directly from the life table itself. The increased understanding and insight into the dynamics of the subject population provided by the table allow us to identify biometrically the stage and factors in that stage that are most likely causative of variability in population density, either Biological Insect Pest Suppression: Applied Quantitative Ecology 45 between or within generations. The process of determining which factor is most closely linked with population density change in a causative fashion is known as key factor analysis (Morris, 1959). Determination of the key factor can be useful in plotting pest control strategy, because, once identified, it potentially permits pre• diction of future population trends (and thus damage estimates) by continuous monitoring of only a single independent variable (Morris, 1959, 1963 b). However, caution must be exercised in applying such methods because in biology, as we know, events do not always follow our mathematical predictions as they do in physics, and key factors may vary from time to time and place to place (Flanders, 1971; Varley et al., 1974). Another benefit derived from life table studies is the availability of a large data base useful in the construction of mathematical popu• lation models. This vast quantity of data is usually best analyzed by breaking it up into interval-specific pieces and constructing submodels for each. These submo• dels may later be combined sequentially to form a comprehensive model of the whole generation (Watt, 1961; Morris, 1963a). Because of the comprehensive nature of the data base, models resulting from it should be more generalistic than others based on less complete data. We also seek the qualities of realism and precision in the model; that is, a close correspondence to, and mimicry of, the observed biological processes and an ability to accurately predict numerical change. Due to the increasing complexities thus introduced, and the need for feedback mechanisms and other interactions, the computer is coming into in• creasing use in this regard. Kenneth Watt from the University of California-Davis is a primary exponent of the use of computers in population dynamics studies and in systems analysis (Watt, 1966, 1968), which he defines as a body of techniques for comprehensive analysis of complex biological problems by viewing them as systems of interlocking cause-effect pathways. Finally, the data provided by life table studies may be used to investigate various ecological processes such as parasitism, predation, intraspecific competition, and the effects of the abiotic influences of temperature or precipitation (Clark et al., 1967). The development of mathematical expressions which describe and mimic these ecological processes will allow their reintegration into the overall population model, and its concomi• tant beneficial refinement. When a workable model is finally derived, it is possible to do simulation studies by adding, subtracting, increasing, or decreasing the value of chosen parameters, and predicting what the effect would be on popula• tion density. We might, thus, for example, detect a weak link in the pest's life cycle and determine at what stage an introduced natural enemy might be most effective, and what kind of enemy it should be. Or we might discover how to manipulate a key factor already present in the environment so that it is more effective. Although population modeling is a powerful tool in biological control, all models are only approximations of reality which may yield more or less useful information. At present, we need more complete knowledge of population dy• namics of pest (and nonpest) insects over long periods in the field, at both high and low densities. No matter how sophisticated the mathematical analysis or the computer employed, the output is no better than the data which are analyzed. To our knowledge, and if we may be facetious for a moment, we are unaware of any records of equations or computers responsible for direct insect mortality; thus the critical need is still to know your insect. 46 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

2.3 Introducing Beneficial Organisms: Questions, Concepts, and Procedures

We have examined the historical development of the various ideas and practices of biological pest suppression (Chap.2.1) and discussed the ecological philosophy which supports those ideas and practices through the medium of quantitative population studies (Chap.2.2). In this chapter we shall attempt to point out and briefly discuss a number of questions which frequently arise in attempting to implement a biological pest suppression program and some concepts and princi• ples which may find application in dealing with these questions. The definition of biological pest suppression adopted by this book includes a number of distinct practices and procedures which are related principally through the fact that they are implemented via human manipulation of a bioecological process of one sort or another. The selection of which process to manipulate is one of the first questions we must address, and the answer we postulate may well determine the ultimate success or failure of the program we devise. Selection of the wrong ecological process for manipulation may lead only to futile efforts at pest suppression. That is why our selection should be more than just a postulate; it must be a decision based on solid factual observation and evidence. Thus, we emphasize the most complete knowledge possible of the target pest and the ecosystem it inhabits. Complete information on the pest, beginning with its cor• rect taxonomic identification and progressing all the way through the studies of its biochemical makeup, promises us the greatest potentiality for locating a weak fiber in the web of processes and events that constitute the life system of its kind. And there is where our attack is concentrated. This is not to say that there must be only a single weak spot and a single strategy for its exploitation. In fact, a number of possible strategies may present themselves, and a prudent combination of two or more in concert may yield results superior to concentration on any single one. Examination of the various techniques of modern biological insect pest sup• pression indicates that the component known as "classical biological control" has the broadest overall potential for use in any pest situation we may face. The majority of the successful programs reported in the literature are classical in nature. Most of the other techniques are powerful tools in selective instances, but are not as universally applicable. Cultural manipulations and the use of pest• resistant hosts are two methods which are potentially useful in many agricultural situations, but their application in practice is still developing or limited to sup• portive stature. Genetic manipulations and the use of pheromones, hormones, and feeding deterrents are methods which, at present, are even more restricted in their applicability, although their potential power is great. Therefore, much of what will follow in this chapter is concerned with the principles and concepts developed in conjunction with the practice of classical biological pest suppres• sion-the manipulation of parasitoids, predators, and pathogens. We do not mean to imply by this that classical biological control methods will be the most effective procedures in every pest situation, but only that the principles are more extensively developed and understood. In fact, the classical practice of introduc- Ecological Compatibility 47 ing exotic beneficial organisms for pest suppression is itself only useful in restric• tive situations. Fortunately, these vulnerable situations are widespread (National Academy of Sciences, 1969a). Introductions of exotic natural enemies are appro• priate only (1) if there exists a vacant niche (or niches) in the life system of the pest which might be filled by the introduced species, or (2) if the present occupant of a niche is an inherently inefficient regulator of the pest and is susceptible to dis• placement by a more efficient introduced regulator. The first situation is most commonly encountered with introduced pest species, and the second with indi• genous pests, but either type of pest may occur in either situation. The discussions which follow are concerned with the desirable attributes of a useful natural enemy, some steps to be taken in introducing beneficial organisms, and a consideration of some basic ecological principles which have bearing on the success or failure of biological pest suppression programs.

2.3.1 Desirable Attributes of Beneficial Organisms

The search for efficient beneficial organisms for use in biological insect pest suppression requires that we have some idea beforehand of what we are seeking. It is generally recognized that there is no sure way of predicting beforehand which species will succeed and which will fail in giving adequate pest suppression (De• Bach, 1964 b, 1974). The answer to this question can be determined with certainty only empirically. However, we can proceed with educated empiricism. Whether we are looking to introduce new natural enemies from exotic locations, or analyz• ing those species which are already present for some way of augmenting their usefulness, we need to know the characteristics which tend to make a species display an efficient regulatory relationship with a pest. Some of these attributes are intuitively discernable in light of the ideas of population dynamics and natural control, and some of them have been recognized only through experience in previous biological control programs. Many of the attributes are closely interre• lated and difficult to separate one from the other, but in general they are as follows:

2.3.1.1 Ecological Compatibility When searching for exotic beneficial organisms for importation against native or introduced pests, it is usually important to seek species whose ecological require• ments are similar to those of the intended target insect. In general, this is done by first accurately identifying the pest and also its probable point of origin if it is exotic, or its geographic distribution if it is endemic. The search can then be concentrated in the native home of the pest or in other areas of the world where it (or a related species) exists in similar ecological situations. Thus it was that C. v. Riley dispatched Albert Koebele to Australia to seek insect enemies of the cot• tonycushion scale (Doutt, 1964), the Canadian government imported paras ito ids from Europe for release against the winter moth, Operophtera brumata (L.) (Gra• ham, 1958b), and the Hawaiian Department of Agriculture (H.K. Nakao, pers. comm., September 23, 1975) brought Ooencyrtus erionotae Ferriere from Guam 48 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

against the banana skipper, Erionota thrax (L.). Parasitoids are frequently limited in effectiveness, at least near the edges of the host's range, by their greater sensitiv• ity to cold, desiccation, heat, etc., and therefore it is important to give strong consideration to species which can withstand such conditions on a par with the host. Disparity in ecological responses may be an important limiting factor in the effectiveness of native beneficial species as well, and an environmental manipula• tion of some sort may be the key to making them into a successful regulative agent. For example, properly timed irrigation of California alfalfa fields enhances the effectiveness of native pathogenic fungi which are otherwise limited by low humidities more than their host, the spotted alfalfa aphid, 1herioaphis maculata (Hall and Dunn, 1957).

2.3.1.2 Temporal Synchronization Closely allied to the ecological compatibility which assures that beneficial organ• isms can occupy the same habitats as their hosts, is a temporal compatibility which brings both there contemporaneously. Benefit derived from natural ene• mies can be greatly reduced if there are areas in space or periods in time which permit the host to escape attack. It is not enough for the pest and its natural enemies to be in the same place at the same time; the life cycles must also be synchronized for adequate regulation to be possible. Thus, the reproductive stage of a successful egg parasitoid must be active at the time of occurrence of the host's eggs in every generation of the host. The efficacy of poorly synchronized entomo• phages may sometimes be improved. For example, manipulation of spring popu• lations of an alternate host could increase the usefulness of Bracon mellitor Say, the most important United States parasitoid of the boll weevil, because it emerges from winter diapause too early to find many weevil hosts available (McGovern et al., 1975). Early season alternate hosts could provide a larger reservoir of parasit• oids to attack later appearing weevils. The practice of periodic inundative release of beneficial insects is another way of artificially synchronizing the occurrence of parasitoid and host.

2.3.1.3 Density Responsiveness We have seen that the processes responsible for effective regulation of insect populations are density dependent (Chap. 2.2). It follows, then, that the most desirable biological control agents will exhibit positive rapid density responsive• ness. Such responses may be of two types: functional or numerical (Solomon, 1949). Functional response refers to the within-generation behavioral activity of the individual parasitoid or predator in increasing its attacks against increasingly numerous hosts or prey. Numerical response refers largely to a multigenerational reproductive increase by the entomophage in response to increasing host density. Although it is generally believed that positive responses of either type are benefi• cial to pest suppression, a strong functional response alone is seldom able to regulate pest densities over many generations (Huffaker et aI., 1971). A rapid and strong numerical response characteristic is the most important attribute of a successful agent of pest mortality, and is in turn dependent on several other characteristics. Dispersal Capacity 49

2.3.1.4 Reproductive Potential One important factor in the display of density responsiveness is high reproductive capacity, through either short generation time, high fecundity, or both. This characteristic is most significant at the time of initial introduction of the entomo• phage when pest numbers are very high in relation to the number of colonized beneficial insects, and at later times, when for some reason, the pest insect popula• tion tends toward escape from established natural control processes. In such unstable situations, high reproductive capacity reduces the lag period before successful reestablishment of subeconomic equilibrium pest density by engender• ing a quick numerical response by the entomophage. In most cases, we seek a parasitoid or predator with an innate potential for increase greater than that of the host/prey, even though that potential may never be realized in practice except, perhaps, for the period after introduction during which the two populations are coming into balance.

2.3.1.5 Searching Capacity The ability to find host/prey at low density has significant bearing on the long• term success of entomophages in the more stable situations which exist most of the time in cases of successful biological pest suppression. Thus, a natural enemy which can destroy pests separated by a large mean distance is more desirable than one which destroys the same percentage of pests existing in closer proximity to each other (Smith, 1939). This points up the fact that the most numerous natural enemy of a pest is not always the most important one in regulating its density. A common entomophagous species may be simply a part of an overall complex of mortality factors which cause a large and consistent reduction in pest numbers. This leaves a small, low-density residual pest population which is responsible for maintaining reproduction of the species. A beneficial organism which can success• fully utilize this low density population and reduce its numbers through efficient searching behavior is a desirable key regulative agent to be sought. A truly ideal beneficial insect would possess both high reproductive potential and good search• ing capacity, but in cases of successful biological control full utilization of the former rarely comes into play because oflow pest densities, and efficient searching ability becomes the primary characteristic because it maintains those low densi• ties.

2.3.1.6 Dispersal Capacity The ability of an introduced beneficial species to easily and rapidly expand its sphere of influence in space to coincide with that of the host is closely tied to its searching capacity and ecological adaptability. Ideally we would like to make one or a few localized introductions of the beneficial organism and let it spread under its own power into the entire range of its host/prey. If the beneficial species is capable of existing in the same climatic situations as the pest, is active in finding and searching all of the potential local habitats of the pest, and displays at some time in its lift cycle an ability to move about in the environment, then adequate dispersal should result. Most good biological control agents show high dispersal 50 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression capability. For example, after the introduction of the braconid wasp, Agathis pumila (Ratzeburg), into Wisconsin against the larch casebearer, Coleophora lari• cella (Hiibner), the parasitoid spread over the entire range of its host at an average annual rate of over 46.7 km/year (Mertins and Coppel, 1974).

2.3.1.7 Host-Specificity and Compatibility Host-specificity is another attribute which may contribute to density responsive• ness. The fact that a parasitoid (or even a predator) is monophagous, or slightly oligophagous, indicates a high degree of biological adaptation to the host, and probably a greater degree of direct and rapid responsiveness to density changes in the population of the target host. Polyphagous species are usually less directly tied to the density changes of a particular component species in their diet, and less likely to be regulative agents. In fact, most cases of successful biological insect pest suppression have been intimately associated with the use of a rather host• specific entomophage (DeBach, 1974). Here again we see the importance ot thor• ough knowledge of the pest and its enemies. An incorrectly identified pest, or inadequately studied parasitoid/predator taxonomy could result in failure to meet host-specificity requirements and, therefore, in unsuccessful biological pest sup• pression. Host-specificity is also closely tied to compatibility or degree of biological adaptation. Monophagous entomophages have usually evolved a high degree of adaptation to the defensive mechanisms of their host/prey which renders all individuals susceptible. However, there are ways in which some individuals may avoid attack by an otherwise useful enemy, resulting in inadequate or incomplete population suppression. Suitable hosts may be separated in time or space, as for example, from an egg parasitoid with an ovipositor long enough to attack only the top layers of the host egg mass. Mechanically incomplete parasitism may occur when an adult parasitoid is not always able to emerge from the host it has killed, as, for example, when a large number of Trichogramma sp. develop in an egg of Pachysphinx modesta (Harris), and the resulting small-sized parasitoids cannot cut their way through the thick chorion (Flanders, 1935). Physiologically incomplete parasitism may result from an abnormally high mortality rate in immature parasitoids, as in the case of Habrolepis rouxi Compere, a parasitoid of the California red scale, Aonidiella aurantii (Maskell). Parasitoids develop nor• mally in scales on yucca plants, but fail to do so in scales on Sago palm (Smith, 1957).

2.3.1.8 Food Requirements and Habits Food requirements and habits are another consideration in choosing a poten• tially useful beneficial organism. A natural enemy which requires only the specific host/prey against which it is released is most useful. Frequently, however, we must assure that suitable alternate hosts are available, or that nectar or pollen sources are present to sustain adult parasitoids. These things can be added to aid an otherwise inefficient native entomophage as well. Some parasitoid species obtain their own supplemental protein by host-feeding on the body fluids of hosts they attack, sometimes killing hosts in addition to those that they actually parasitize Steps in Establishing a Biological Control Program 51

(Campinera and Lilly, 1975). Other entomophages can sustain life through pe• riods of low host/prey availability by resorbing their own eggs (Flanders, 1942). Some lacewings require a source of protein such as pollen-honeydew or prey before they can successfully reproduce (Tauber and Tauber, 1974). Useful parasit• oids usually display powers of host discrimination such that they avoid superpar• asitism, and thereby, in effect, increase their fecundity by distributing their re• productive capacity among more hosts. For example, a host marking pheromone is produced by Telenomus sphingis (Ashmead) which reduces the chances of exces• sive numbers of parasitoid larvae in a marked host egg (Rabb and Bradley, 1970).

2.3.1.9 Hyperparasitism

A negative attribute to be avoided in selecting biocontrol agents is the incidence of hyperparasitoids, detrimental diseases, or predators. Hyperparasitoids are the most frequent and important of the three, and most beneficial organisms are thoroughly screened in the insectary before their release, in order to eliminate any secondary parasitoids which may be present. In order for an entomophagous species to fully realize its potential against its target, it must be free from natural enemies just as the pest insect was unrestrained by natural enemies and free to become a pest. It is possible, for instance, that a mediocre entomophage attacked by hyperparasitoids in its native environment, could be freed from such restric• tions in the insectary, and become an important pest-regulating agent when re• leased in a new hyperparasitoid-free environment.

2.3.1.1 0 Culturability

One final attribute which may be important in using an entomophagous species for pest suppression is the ease with which the organism can be mass-reared (Doutt and DeBach, 1964). If the species can be collected in its native home in large numbers, such qualities may not be important, and importations may be on a one-to-one capture/release basis. But frequently only small numbers of the desired species are available in the native environment, often because it effectively holds the host/prey population at low density. In these cases, an adequate size colony for introduction must be built up in the insectary, and the species must be amenable to lab-culture. Elimination of hyperparasitoids also sometimes requires at least one generation of lab-culture, and parasitoids and predators used in inundative release programs must be easily mass-reared.

2.3.2 Steps in Establishing a Biological Control Program

The potential need for a biological pest suppression program is established when it becomes evident that the activities of an insect population are causing economi• cally significant damage. With regard to the beneficial organisms in particular, we must decide what tack the program should take. We first try to determine if the pest is a "real" pest species, or if it is, in fact, a man-made pest generated by the use 52 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression of pesticides or some other upsetting agency. In the case of a real pest we can begin, usually immediately, to consider the importation and release of the natural enemies whose absence is evident. This is the subject we shall discuss herein. In the case of man-made pest, the natural enemies are (or were) usually al• ready present, but their effectiveness has been destroyed or impaired by adverse human activity. There may be no need to establish new suppressive agents if the beneficial effects of those already present can be restored or improved through the conservative practices and manipulations discussed in Chapter 4.2. At present, the most important of these is care in the use of pesticides. Repairing the damage done to populations of natural enemies through human activities may be speeded up through augmentation of their numbers with mass releases when the detrimen• tal activities are suitably modified. If, on the other hand, the practices at fault cannot be changed, it may still be possible to maintain biological suppression (1) by periodic colonization of suitable beneficial organisms, (2) by altering the genetic constitution of the present natural enemies so that they will again fit into the ecosystem, or (3) by considering the importation and release of some new agents which will satisfactorily regulate the pest in the new ecosystem. Thus, man• made pests are often vulnerable to introduced natural enemies also. Real pests are most frequently exotic species which have become established locally without their normal complement of natural enemies, and the common biological control practice is to construct a complex of natural enemies which can regulate the pest's population at subeconomic densities. The natural enemies are most often of foreign origin also, and the regulative system they compose will most often be at least a partial reconstruction of the natural enemy complex in the native home of the pest. Other variations on the basic geographic idea of using exotic natural enemies against exotic pests may be used, however. For example, exotic natural enemies originating in ecosystems similar to that of the pest, and perhaps attacking ecologically or taxonomically similar host/prey species, may be employed against native man-made pests. Native beneficial organisms may be moved from one part of a country where they are active and effective to another part where they are absent. Or, finally, endemic natural enemies may be collected, mass-produced, and released in in un dative numbers against native pests. Once the need for introducing beneficial organisms has been determined, the program may proceed as follows:

2.3.2.1 Exact Identification of the Pest As indicated previously, identifying the pest is the first step in determining if action is required to protect against pest depredation. This includes recognizing that damage is occurring, determining the specific cause of the damage, and precise taxonomic identification of the pest insect. Recognizing that preventable economic injury is occurring may not always be easy, if the damage is consistently present and accepted. Unless careful observation is made, damage may be attri• buted to the wrong cause and inappropriate action taken. Thus, for example, we might attempt to protect a crop from extensive defoliation apparently caused by a few obvious caterpillars, when in fact, the real problem results from much more numerous nocturnally active species which hide underground during the day. Host-Parasitoid Lists and Other Faunal Surveys 53

Once the blame has been properly placed, an exact taxonomic identification of the pest is the key to further progress (Sabrosky, 1955; Rosen and DeBach, 1973). The species name gives us access to the available literature on the pest and what is already known about it. In addition, we can also explore the possibilities of utilizing the natural enemies of related species.

2.3.2.2 Origin, Geographic Distribution, and Ecological Requirements Once the exact identity of the pest is determined, we can turn to the literature of economic entomology for important information on how to proceed further in its biological suppression. Perhaps we may find that the species has been the subject of successful programs elsewhere, and similar procedures might again be usefully employed. For example, once the vedalia beetle suppressed cottonycushion scale in California, it was used with similar success almost everywhere else that the scale was a pest of citrus (DeBach, 1964b). If no precedential work has been done on the target pest, then perhaps techniques and/or natural enemies are available from work with similar or related pests. Finally, we may have to settle for infor• mation on the previously known geographic distribution of the pest, and hence its probable origin. By examining its previous distribution and the ecological condi• tions under which it survives, we can get some idea of the pest's potential range in our area. Examination of the degree to which the species is a pest in its homeland indicates whether or not natural control agents exist in that environment which might be suitable for introduction against the escaped pest in our area.

2.3.2.3 Host-Parasitoid Lists and Other Faunal Surveys If, as is frequently the case, the target species is not an important pest in its place of origin, there is good reason to believe that at least one species of density• dependent natural enemy is present there, and is responsible for regulating the population size. If the species is a pest, there may still be a potentially useful agent present which, when moved to the new environment, free of its own natural enemies, can regulate the pest population at low densities. In any case, we may save a lot of preliminary field work aimed at identifying candidate entomophages by searching the literature for previous specific studies of the insect species and its natural enemies in the home distribution. Even if no survey has been done pre• viously on the insect species of specific concern, one can turn to lists, catalogs, or area-wide faunistic surveys which are available for many regions, and which frequently at least list diseases, parasitoids, or predators which are present. Unfor• tunately, many of these catalogs are arranged according to the names of the entomophages, with no cross-reference allowing one to locate the parasitoids and predators through the name of the host. 1he Catalogue of the Parasites and Predators of Insect Pests, prepared under the direction of W. R. Thompson (1943- 1965) by the staff of the Commonwealth Institute of Biological Control, is most useful in this regard because of its division into four sections: The first and third allow access to the parasitoids through their hosts and the predators through their prey, respectively, and the second and fourth give access to the hosts through 54 Historical, Theoretical. and Philosophical Bases of Biological Insect Pest Suppression their parasitoids and the prey through their predators, respectively. The Thomp• son catalog is only a list compiled indirectly from the world literature of economic entomology as it was abstracted in the Review of Applied Entomology through 1937, but it is an excellent place to begin a search for useful beneficial organisms. Recently, Herting (1972) has compiled a sequel to the Thompson catalog, with a broader scope, including references to parasitoids and predators of all of the terrestrial arthropods as they appeared in RAE from 1938 through 1962.

2.3.2.4 Field Study of both Target Insect and Beneficial Organisms Once the literature survey is complete, we know with some assurance, where to go in the world to find the target species, what its pest status and ecology are there, and what its recorded natural enemies are. Additional field studies may be needed in the native habitat to fill gaps in the knowledge thus accrued, and to make easier the specific task of collecting sufficient beneficial organisms for shipment. Under• taking field investigations also gives an opportunity to select the most suitable collecting areas for obtaining large quantities of parasitoids or predators, and for conveniently moving them from the field to the point of shipment. Collecting areas are usually chosen for their climatic and ecological similarity to the in• tended new environment, and for the presence of a "good" candidate entomo• phage as evidenced by a low target insect density. A final benefit of preliminary field studies of the target insect and its natural enemies is to corroborate the presence ofthe beneficial species listed in the literature and familiarize the foreign collector with their recognition. Such familiarity is important because we need to know with great certainty the identities of beneficial organisms which we intro• duce (Clausen, 1942), not only to assure that we know what to look for when assessing establishment after introduction, but also to make sure that we recog• nize and screen every potentially useful biological agent, even morphologically similar sibling species (Rosen and DeBach, 1973). In addition, the identification and screening process allows us to avoid wasting time on beneficial species which may already be present in the intended area of introduction, and to avoid the introduction of potentially inimical species such as hyperparasitoids.

2.3.2.5 Prediction of Success and Efficiency This subject is mentioned here only briefly, but is discussed in more depth later (see 2.3.2.10). Despite the great advances in biological insect pest suppres• sion, and its many successful applications, it is still essentially impossible to predict with certainty the outcome of any program before it is carried out. The greatest assurance of success probably lies in introducing a beneficial organism which has proven itself before against the same target pest in a similar environ• ment elsewhere (e.g., P. berlesei used in various countries against the white peach scale, 2.1.2). It is still important to gain as much preliminary knowledge as possible about ecological compatibility, behavior, synchronization, biotypes, and all the rest, but in the final analysis the only way to determine what effect a beneficial organism will have on pest density is to introduce it. Shipment of Beneficial Organisms 55

2.3.2.6 Collection of Beneficial Organisms The major concern of collecting beneficial organisms for importation is usually to get as many as possible in the briefest time possible. The techniques employed must usually be tailored to the specific pest and its natural enemies, the availabil• ity of manpower, and sometimes the terrain. Frequently individual hand-collect• ing of predators or parasitized hosts is the only feasible method, but other meth• ods may be employed. For example, one might employ the host exposure method in which an artifically dense population of hosts is encouraged or created in a controlled area subject to exposure to the desired parasitoid. After a sufficient degree of parasitization has occurred the hosts may be easily regathered and shipped. Collection sites in the exporting country need not necessarily be remote, exotic, or inaccessible. In fact, it is usually best that they be convenient to the central point of export. Often the best collecting may be found in door yards, parks, or along roadsides. If the intended target insect is a pest of an agricultural crop, then it may be wise to collect beneficial organisms which attack it in agricul• tural plantings in its native home, on the assumption that they may have adapta• tions most suited to the invaded area (National Academy of Sciences, 1969a). The duration and geographic scope of the collection process should be as broad as possible. While it is true that some successful programs have been accomplished using representatives of one or two beneficial species collected from a single locality over a brief period of time, greater probability of success is likely with a more extensive effort. For example, the collection projects of the CIBC are usually directed from permanent field stations, and carried out over the entire distributional range of the pest insect if possible. Collection of natural enemies extends over at least one full season of pest activity in order to sample the full complex of beneficial species from all life stages of the pest.

2.3.2.7 Shipment of Beneficial Organisms Operationally, one of the most critical steps in carrying out a beneficial organism introduction program is transporting the parasitoids or predators from the place of origin to the place of introduction. We have seen that a considerable expendi• ture of time and effort is already invested in the entomophages by the time they are ready to ship, and it is only sensible to accord to them an amount of care and expense in shipping commensurate with their value and difficulty of replacement. In the early history of biological control, transporting beneficial organisms fre• quently involved shipboard transits of several weeks' duration. With little or no refrigeration to suspend activity, it was often necessary to provide food and water to sustain life during the long journey, and sometimes this even involved trans• porting living host/prey insects on potted plants. Needless to say, the entomolo• gist collector often accompanied his charges on the journey to assure their ade• quate care. The use of modern air transportation has greatly benefitted biological insect pest suppression. International air service is available to most major cities of the world, with national air service links to other centers within each country. When using air transportation for shipment, personal contacts with airline and/or postal officials 56 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression are advisable to avoid unnecessary delays and other hazards (National Academy of Sciences, 1969a). The requirements for shipping live insects are similar in many ways to those for any perishable goods, and the difference between success and disaster may lie in the "personal touch" from delivery to the carrier to pickup at the receiving end. Every attempt should be made to schedule the most rapid practical transfers throughout the trip, and to maintain the shipment within a reasonable temperature range at all times. Constant telephone or cablegram com• munication between shipper and recipient assures coordination and anticipation of activities. Shipments should be timed, when possible, to arrive on weekdays and during regular office hours. The container used for shipment must be strong enough to survive rough handling and constructed so as to prevent the escape of any insects which may be active en route. Many containers are constructed of wood; they often provide some air ventilation, controlled humidity, and sometimes a means of customs inspection. Modifications may sometimes be necessary to provide food require• ments, especially if the trip will last more than 2-3 days; honey or honey mixtures are the most common nutrient and moisture sources used for this purpose, either in the form of honey streaks inside the container or honey impregnated excelsior. It is sometimes necessary also to separate individuals within the shipment to prevent cannibalism or injury due to aggressive or protective behavior. We may simply provide increased perching surface with excelsior packing, or confine the entomophages to individual cages or gelatin capsules. Cardboard mailing tubes or aerated plastic containers may be suitable for airmail shipments under moder• ate conditions, but vacuum flasks or foam-insulated containers may be necessary to maintain the contents of shipments at lowered temperatures if they are poten• tially subject to exposure to lethal heat levels. Containers should be suitably labeled to caution against temperature extremes or other adverse conditions. Although insects can be shipped at any stage of development, the resting stage is usually the easiest to handle. Because of the rapidity of air transport, there is little chance of transformation from one stage to another during transit. Predators are usually sent as fully fed adults, whereas parasitoids are shipped in host materi• al, part of which is known to be parasitized, or as cocoons (Hymenoptera), pu• paria (Diptera), or adults. An information sheet should be a part of each shipment indicating at least the identity and source of the enclosed material, the number of predators, parasitoids, or parasitized hosts shipped, and the dates of collection and shipment. The move• ment of living insects of any sort into (or even within) many countries is usually restricted or controlled to some degree by plant- and animal-protection officials. For example, in the United States, two Federal statutes prohibit the importation and movement of plant pests, pathogens, vectors, and articles that might harbor these organisms unless authorized by the United States Department of Agricul• ture's Animal and Plant Health Inspection Service (Anonymous, 1975a). "Autho• rization" comes in the form of a permit to import living pest organisms or ship them in this country. APHIS carefully weighs risk against expected benefits before issuance of such a permit. Organisms not requiring a permit include pure colonies of plant pest predators and parasitoids, pure cultures of plant pest pathogens, and non pest species. However, agencies responsible for importation of beneficial or- Quarantine 57 ganisms generally acquire a permit whether the colony is "pure" or not, and suitably affix it to the outside of the shipping container. Finally, it is usually wise to send material in a series of small shipments rather than in a single large one, to minimize the possibility of losing them all due to an unusual delay or other chance adversity. If communication lines are open be• tween recipient and shipper, notice can be given of problems which may arise, and suitable adjustments made in packaging or scheduling to reduce mortality m subsequent shipments.

2.3.2.8 Quarantine

A beneficial organism introduction program should not be attempted without access to adequate quarantine facilities. It is possible to process the material for introduction in quarantine facilities in the country of origin, and then release the output directly, as received, in the importing country, but in most cases imported material is received in a quarantine laboratory. The purpose of quarantine is twofold: first, the procedure prevents the premature escape of the imported in• sects, and secondly, it prevents the contamination of entomophage cultures by native species. Preventing the premature escape of imported insects is important not only to assure that the greatest number of the imported beneficial species is retained for release where they are needed, but also to allow adequate screening of the ship• ment before release to eliminate hyperparasitoids, unwanted contaminating spe• cies, and diseases which might reduce the effectiveness of the introduction. Screen• ing is often accomplished by rearing the imported species for one or more genera• tions under controlled conditions. Thorough knowledge of the identity and range of useful habits of the insects is required before we can confidently decide that the species under culture is the one we want to release, and that it is free of contami• nation. It is likely to be impossible to undo an introduction once a species is established, so extreme preliminary caution is required. Most countries have a single central quarantine facility through which all imported biological control material must pass before it is released. In the United States, with few exceptions, the U.S. Department of Agriculture'S Beneficial In• sects Research Laboratory in Newark, Delaware, is responsible for this function, although three states (California, Florida, and Hawaii) which are actively involved in biological insect pest suppression have their own approved quarantine laborato• ries. In Canada, beneficial organisms arrive at the Canada Department of Agricul• ture's receiving station in Ottawa, Ontario. Facilities used for quarantine (Fig. 10) are usually specially designed for this function and feature insect -tight construction with such things as triple-glazed windows, double-sealed air lock doors, closed-air ventilation systems, and special systems of illumination which discourage the passage of insects through exit doors. Most laboratories also include specialized rearing facilities for propagation of beneficial organisms, and fumigation and incineration capability for treating shipping containers and rearing cages. Admit• tance is usually restricted to authorized personnel only, and special laboratory coats and caps are often required within the facility but must be removed before leaving. 58 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

2.3.2.9 Propagation It is probably most advantageous to introduce large numbers of beneficial organ• isms which have been collected and shipped directly from the field. However, sometimes it is necessary to propagate the collected stock and multiply its num• ber in the laboratory, especially when only a few individuals are available from the donor country (Simmonds, 1966). The former method is usually the most economical, involving much hand labor but little in the way of expensive equip• ment. In addition, the whole parasitoid and predator complex can be gathered and shipped with little added effort. On the other hand, reliance on field collected material increases the chances of importing unwanted or even detrimental species, and subjects the introduction program to greater chance of abortion through accidental loss of materials in transshipment. The method of laboratory propaga• tion from a small initial stock is usually far safer when carried out under suitable controlled conditions. Emphasis may be placed on accumulating a particularly desirable beneficial species. Synchronization of the entomophage and pest life cycles may be increased by carefully timed propagative output, and, perhaps, by rearing the beneficial organism year-round and storing the progeny produced until the proper time for release. Propagative increase of beneficial insects fre• quently involves extensive investment in rearing facilities and equipment, and often considerable labor costs (Fisher and Finney, 1964). It requires complete knowledge of life cycle, biology and behavior, proper rearing conditions, and a suitable laboratory host or artificial diet (Finney and Fisher, 1964). The intended target pest is the preferred laboratory host in order to accustom the introduced species to it, and assure that no unforeseen detrimental relationships or poorly adapted cryptic races of the beneficial organism are present. The primary concern is for ease in handling and production. If the intended natural host is not amena• ble to laboratory handling, or is unavailable during certain periods, then a facti• tious (unnatural laboratory) host may be used. For example, Brachymeria inter• media (Nees), a pupal parasitoid of the gypsy moth, is reared in the laboratory in pupae of the greater wax moth, Galleria mellonella (L.) (Anonymous, 1973a).

2.3.2.1 0 Release and Colonization Once we are assured of the safety and suitability of imported beneficial species, by either carefully screening field collected material or by controlled laboratory propagation, we are ready to attempt establishment in the field. The current trend is toward the earliest possible attempt at field release. First of all, early establish• ment will reduce the need for extensive laboratory propagation but will still provide a local source of material for additional introductions at other loci. Secondly, years of experience seem to indicate that only a minimal colonization effort is required to establish natural enemies which will eventually become im• portant and effective suppressive agents (Clausen, 1951). As methods and skill in determining the safety of imported material become more efficient, and the tech• nologies of handling and transportation improve, the method of direct release should increase in importance. Over the years, a knowledge of the most suitable conditions for establishing imported beneficial organisms has been empirically accumulated. Failure to with- Release and Colonization 59 stand various climatic extremes in the new environment frequently has proven to be a limiting factor, but other problems may also arise. Other physical factors such as the topography or intensity of agriculture may prove unsuitable. Incom• plete understanding of the host-parasitoid or prey-predator relationship may lead to the introduction of a poorly adapted beneficial organism, or perhaps one which was misidentified and is wholly unsuitable. Sometimes the intended host/prey may have become genetically insulated from the entomophage in the new envi• ronment, even though it is susceptible in the country of origin (Wong, 1974). Alternate hosts, required food supplies of nectar or pollen for the adult, or other necessary environmental elements may be missing from the introduction point, and deter establishment of the entomophage. Proper timing of the introduction is also important, especially if the target insect is distinctly univoltine. Parasitoids frequently require a preoviposition period after emergence and mating, which must be taken into account in order to synchronize released material with the life cycle of the target pest. Sometimes it is important that a particular host instar be prevalent in the field at the time of release. Predators should usually be released as adults for the greatest assurance of ease in finding a mate and early reproduction. Based on the preceding information it is usually possible to select one or a few promising sites for introductions, which seem to fulfill the known requirements of the entomophage and allow for easy natural or artificial spread. Frequently, colonization is done within field cages, especially when dealing with predators, to minimize initial dispersal and protect against native competitor species. Once the colonized entomophage is established in a field cage and reproduction has begun, the cage may be removed. Particular attention should be given to weather conditions at the time of release. Releases should be withheld in deference to predicted frosts, heat waves, heavy rain or winds, or any other conditions which could cause high mortality of colonized insects. Bright sunlight often stimulates rapid and undesirable dispersal and should generally be avoided. Releases are probably best made in either early morning or late evening, when light levels are subdued, temperatures are lower, and humidity is high. Under such conditions dew on the vegetation is available to the insects, and the other conditions discourage dispersal, making mating more likely, and concentrating ovipositional efforts. The number of individuals which must be released to achieve establishment is another subject which defies predictability (Turnbull and Chant, 1961; DeBach and Bartlett, 1964). Ordinarily, it is probably wisest to release larger colonies at a few points than to dilute the available release stock over a large area. However, it is also a good idea to make introductions in localities that represent the full range of environmental conditions under which the target pest insect exists. Very few species of beneficial insects can be expected to regulate their host over its entire range, but multiple introductions will most quickly present the spectrum of avail• able conditions for selection. The final decision on how many individuals to release in how many areas may frequently be dependent upon the numerical availability of the beneficial species. For example, the cocoon parasitoid of pine sawflies, Dahlbominus juscipennis (Zetterstedt), was released by the hundreds of millions in many localities at a rate of 10000 individuals per colony. On the other hand, parasitoids such as Opius ilicis Nixon, which attacks the holly leaf miner, 60 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

Phytomyza ilicis (Curtis), have been established from a single release of ten indi• viduals (McLeod, 1953). Parthenogenetic species can be released in smaller colo• nies than can sexually reproducing species. The influence of the number of beneficial organisms released on success in establishment was most recently discussed by Beirne (1975). He analyzed the introductions of 159 species made into Canada for which results are known, and concluded that "the greater the number released the greater the likelihood of successful colonization and that if the numbers were below some minimum (about 5000 individuals) the probability of success was small." The analyses also indi• cated that the greater the number of individuals per release (about 800 minimum) and the greater the number of releases per species, the greater the possibility of establishment. The greatest success was achieved from the smallest releases in the stable and discrete orchard environment; lesser success was attained with larger numbers released in the stable but diverse forest environment; the lowest rate of success occurred in the unstable monoculture of annual agricultural crops, even though the largest numbers per species were released in that environment. A really effective imported natural enemy will become established easily and rapidly, usually within the first year (DeBach, 1974). Most past experience with introduced beneficial species seems to support the conclusions of Clausen (1951), who suggested that, with suitable conditions, if establishment is not evident within three years after releases are begun, then there is little hope of success. McLeod (1962) suggested a five year release period might be required. Both Thompson (1951 a) and Sellers (1953) warned against blindly accepting such hy• potheses. There are some exceptions; for example, the sawfly cocoon parasitoid, Pleolophus basizonus (Gravenhorst), was not recovered in some areas for 12 years after its last release (Beirne, 1975), and Macrocentrus grandii Goidanich, a bra• conid parasitoid of the European corn borer, O. nubilalis (HUbner), was not recov• ered for nine years after its last release in Wisconsin (Mertins and Coppel, 1974). In general, after three years with no establishment, introduction efforts would be better spent on other species, or perhaps on different strains of the unsuccessful speCIes. A final, and very important, step in releasing beneficial organisms into a new area for biological insect pest suppression is the deposition of voucher specimens in a permanent and reputable insect collection (Sabrosky, 1955). Voucher speci• mens are representative examples of the actually released entomophage stock made available as a reference for comparison when recovery collections are made, or should any question arise later about the true identity of introduced material.

2.3.2.11 Follow-up Recoveries An introduction program is not complete until we have determined the establish• ment of the introduced beneficial species and its rate of dispersal. This is usually done by making field observations and collections in and near the site(s) of release. The presence of the introduced species may be determined visually in the field, by dissection of parasitized hosts, or by rearing adults from field collected host material. The first such efforts may be made after the presumed time of one generation in the field, but establishment is not proven until recoveries are made Evaluation 61 after a complete year has passed, including the (possibly) limiting season of the locality (i.e. cold winter, hot dry summer, rainy season). Recoveries made in the former instance indicate temporary or initial establishment, those in the latter indicate that permanent establishment is likely. DeBach and Bartlett (1964) sug• gest that an insect is permanently established only if it is recovered in three successive years after its release. After the initial qualitative determination of the simple presence of the introduced entomophage, we may wish to determine its rate of spread from the point of establishment. This can usually be accomplished by applying the same methods used to determine establishment, but the sampling is done at various distances from the release site along predetermined transect lines or a grid pattern. Thompson (1951 a) attempted to treat the dispersal prob• lem theoretically, and concluded that the rate of spread from the initial point of release might not be as rapid as one would empirically expect. A new and, as yet, unproven technique for determining the presence and establishment of introduced entomophages is now under study in Wisconsin. Preliminary experiments indicated that the localized presence of the ichneumonid sawfly parasitoid, Exenterus amictorius (Panzer), could be easily detected through the use of live virgin female parasitoids as bait in sticky-traps suspended in pine trees. Male E. amictorius were readily attracted to the females and caught in the traps. We are attempting to adapt the method for use in recovery of other recently introduced parasitoids, such as B. intermedia.

2.3.2.12 Evaluation The final stage of a natural enemy introduction program is the assessment of its effectiveness. It is only by careful and continuous monitoring of the increase and spread of introduced entomophages, and the exact evaluation of their importance as regulating factors that biological pest suppression can rise above crude empiri• cism (Thompson, 1951 a). A common criticism is that too many programs are conducted on empirical grounds, and thus, the conclusion of one project, whether successful or not, does not add significantly to our knowledge of population phenomena and how they are modified so that the next project may start from a more enlightened level (National Academy of Sciences, 1969a). Until we can explain why an introduction program is a success or a failure, biological insect pest suppression will remain an art not a science (Krebs, 1972). There are basically three satisfactory ways of evaluating the effectiveness of entomophagous species: (1) qualitative analysis, (2) experimental exclusion pro• cedures, and (3) quantitative evaluation (DeBach and Bartlett, 1964; National Academy of Sciences, 1969a). The qualitative approach to analysis of effectiveness of introduced natural enemies is the easiest, quickest, and most widespread method in use. It cannot prove that successful biological pest suppression has taken place, and, in fact, may provide misleading results; however, when properly interpreted this method can yield strong indications as to the outcome of a release program. The procedure involves frequent extensive samples and observations of the progress of the intro• duced species in establishment, spread, and apparent cause--effect relationship to declining pest populations. Thus, if we observe that establishment of the intro- 62 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression duced species is followed by its increase in numbers at the expense of the pest, and the pest population obviously decreases at every point to which the introduced species disperses, then we have established a probable cause--effect relationship. A continuing low pest population and repetition of this pattern in other countries where the beneficial organism is introduced is additional evidence in support of success (Flanders, 1959a). The major detracting feature of this qualitative ap• proach is that the mortality caused by an introduced entomophage is not neces• sarily indicative of its importance in regulating the pest population. A newly introduced entomophage may provide a large apparent degree of mortality, but such mortality may simply replace that caused previously by other factors already present. An effective introduced species will provide at least some mortality in addition to that already occurring and, although the incremental increase may not be large, it can be the significant addition necessary both to reduce the population density of the pest to a subeconomic level and keep it there. The true importance of an introduced beneficial species to pest population suppression, and thus the success of the introduction program, can be proven through the use of some type of natural enemy exclusion technique (DeBach and Huffaker, 1971). An attempt is made to compare the population density of the pest in the absence of the newly introduced beneficial organism with that in the presence of the introduced species. This is done in retrospect by monitoring two parallel plots (or sets of plots) which differ only in the exclusion of the natural enemy from one plot. Thus, after a period of time we can directly determine the actual effect of a parasitoid or predator by observing how the pest population protected from it increases as compared to a nearby similar unprotected popula• tion. One way of excluding beneficial organisms is by mechanical means. For example, we might employ cages, sticky barriers, air currents, or hand picking to exclude all natural enemies, or perhaps only a certain selected species (National Academy of Sciences, 1969a). DeBach et al. (1951) employed a special type of exclusion which they called the "biological check method," in which ants were used to protect honeydew producing citrus scale insects from their natural ene• mies. Another way of excluding beneficial organisms from a test plot is by chemi• cal means. It is not difficult to find pesticides which are very toxic to parasitoids and predatory insects but have little effect on more resistant pest species, espe• cially at low dosages. Frequent application of such chemicals can virtually elimi• nate beneficial organisms from the treated area without noticeably affecting the target species which is then free to multiply unrestrained. Suggestions that the chemical treatment might somehow directly stimulate the pest to increase in numbers may be overcome by applying the toxic chemical to a border area surrounding the test plot, thus killing any mobile beneficial organisms moving into or out of the central core area and eventually reducing their numbers greatly, while avoiding actual treatment of the pest (DeBach and Bartlett, 1964). Perhaps more than any other approach, this type of experimental evidence should con• vince skeptics of the validity of pest suppression by biological means. The final approach used to determine the effectiveness of an introduction program is quantitative mathematical analysis. This procedure involves the most effort of the three, but also yields the best proof of success or failure in attaining our goal and the most information about why the program succeeded or failed. Situations Where Biological Pest Suppression Applies 63

Essentially, the method involves the development of extensive life table informa• tion about the pest's life system both before and after the introduction of benefi• cial organisms (National Academy of Sciences, 1969a; McLeod, 1975). To gain a true picture of the effect of an introduced entomophage we must have baseline life table data about the pest population before the parasitoid or predator introduc• tion for purposes of comparison. The exclusion techniques discussed in the preceding paragraph crudely attempt to provide this kind of comparative data in retrospect, and may also be used to study the effects of endemic natural enemies. Preintroduction population dynamics studies and life tables give us an indication of the long-term equilibrium density of the pest and what factors are important in determining that density. After introduction of a new biological control agent, similar studies will indicate quantitatively whether a new, hopefully lower, equi• librium density has resulted, and what factors are responsible for maintaining the new density. A comparison of the two sets of data will show any differences between them, and particularly whether the introduced species is causing mortal• ity in lieu of other factors or is producing important additional mortality. It has even been suggested (National Academy of Sciences, 1969a) that increasingly sophisticated methods of population modeling and computer usage may soon allow us to simulate this type of pre- and post introduction life system data before actually trying the introductions in nature, with mathematical expressions repre• senting different species of natural enemies and different introduction strategies.

2.3.3 Basic Ecological Principles Bearing on Biological Insect Pest Suppression

If we consider biological insect pest suppression to be a form of applied ecology (Chap.2.2), then it follows that its successful practice is governed by our under• standing of a number of basic ecological principles. In fact, the philosophical basis of biological control is founded on the belief that the density of many pest species is subject to reduction by ecological manipulation of suitable biological and environmental processes to make them less hospitable to the pest. We mention or discuss some other important ecological concepts at appropriate places through• out other chapters, but here we will reemphasize several of them and introduce some others not covered in other connections.

2.3.3.1 Situations lthere Biological Pest Suppression Applies

Like other methods of insect pest suppression, the biological control method is not a universal panacea. There are certainly many pest situations in which this method alone is incapable of providing adequate protection from economic loss. On the other hand, there are probably few pest situations in which, when ade• quately studied, biological methods could not contribute substantially to reduc• ing pest density, perhaps in integration with one or more other methods. Biologi• cal insect pest suppression should not be discarded a priori as impractical or not applicable in any situation, but should be considered as a desirable goal in each until proven unsuitable for the particular problem at hand. As we become more 64 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression and more cognizant of the importance of natural control in preventing the major• ity of insect species from attaining pest status, it becomes increasingly apparent that no strategy of existence is completely immune to outside regulation. No matter what the pest, where it originates, where it lives, or what it does, some natural enemy is likely to have developed specialized adaptations to enable it to attack the pest. As we have seen, introduced alien pests are obviously the most likely candi• dates for biological suppression by the importation of natural enemies. The suc• cess of this approach has been documented many times over (DeBach, 1964a; Huffaker, 1971 b; Sailer, 1972; Commonwealth Institute of Biological Control, 1971; etc.), however, native pests have also been successfully suppressed with imported natural enemies (Taylor, 1937; Drooz, 1960), and should be considered as possible targets as well. The imported beneficial organisms in the latter case may be previously associated with the target species in another country, or, more commonly, may attack a related species or one which inhabits the same micro• habitat (Pimentel, 1963). The indigenous pest which is amenable to biological control is either without many natural enemies, or exists in an environment where its effective natural enemies have been destroyed or inhibited by human activities. In either case we may find effective beneficial organisms elsewhere which can be successfully established in the pest's habitat and reduce its density. Or, in the latter case, we may be able to encourage the indigenous natural enemies through environmental manipulations to once again regulate the pest population at low densities. Franz (1970) discusses what he calls "adaptation importation" which refers to the special case in which native organisms accept and attack a newly introduced pest species, and are subsequently introduced into the original faunal region of the pest in hopes that they will do the same there. A new concept in beneficial insect introduction is now under development in Wisconsin. The State is currently threatened with imminent and inevitable inva• sion by the gypsy moth, Porthetria dispar (L.), a serious forest defoliator. An effort is under way to increase the environmental resistance of Wisconsin forests to invasion by the moth by establishing some of its associated polyphagous paras it• oids on indigenous alternate hosts (see 2.3.3.4). Then, when P. dispar does arrive, its natural enemies will already be present and well established, avoiding the usual temporal lag in their appearance in newly invaded areas, and perhaps preventing the pest from reaching outbreak proportions. The suitability of biological suppression methods for "direct" pests (as op• posed to "indirect" pests) was questioned by Turnbull and Chant (1961). Direct pests cause immediate economic loss at low population density by directly attack• ing a marketable item such as a fruit; indirect pests can be tolerated at higher densities because they only indirectly affect marketable produce by reducing overall growth and vigor in their host through generalized attacks. Huffaker et al. (1971) suggest that the olive scale, Par/atoria oleae (Colvee), is a direct pest of olives in California which was successfully suppressed by an introduced parasitoid, Aphytis maculicornis (Masi), showing that such pests are suitable targets. De• Bach's (1974) assessment is probably most accurate, concluding that the ex• tremely low population densities required to offset the economic effect of direct pests makes them less likely, but not impossible, subjects for biological suppres- Multiple Species Introductions and Competitive Displacement 65 sion. This subject may also be approached on the basis of the ability of the host to withstand damage by the pest. Thus, some crops such as forest trees, forage plants, and ornamentals can usually sustain considerable pest populations and injury levels before the economic threshold is reached. On the other hand, a single insect per plant might conceivably cause economically important damage to certain fruit or vegetable crops. Lloyd (1960) has suggested that it is the stability of the environment associated with perennial host plants that encourages success• ful biological suppression of their pests. There is probably a certain amount of validity to this hypothesis, but Turnbull and Chant (1961) successfully argue that the more important characteristic of such host plants is their degree of tolerance to injury. In summary, we may suggest that the best prospects for biological suppression are indirect pests of hosts which can tolerate relatively high pest density and which have a high economic injury level. However, no crop or pest insect may be rejected out-of-hand as unsuited to the biological method of pest suppressIOn. Finally, there is Taylor's (1955) contention that tropical pests and those occur• ring on islands or within other geographicaily or ecologically restricted areas are more susceptible to biological suppression than are pests in temperate regions or continental areas. Past experience seems to lend some support to these observa• tions, particularly the "island concept," but there are too many exceptional exam• ples of success in temperate and large continental regions to allow statement of this hypothesis as an irrefutable law. Again, each pest problem must be analyzed on its own merits.

2.3.3.2 Multiple Species Introductions and Competitive Displacement Another unsettled issue in biological insect pest suppression is whether we may expect better results through the importation and release of several species of beneficial organisms or by searching out and releasing what we believe to be the one "best" species. Among those supporting the single species philosophy are Turnbull and Chant (1961), ZwOlfer (1963), Watt (1965), and Turnbull (1967). They feel that only the most promising beneficial species should be introduced to avoid potential adverse competition between natural enemies. Bringing in the species one at a time allows for analysis and evaluation of their individual contribution to density regulation and comparison with their predicted value. Individual species may be introduced in sequence until the one "best" species for pest regulation is found, and then further introductions are considered superfluous or even detrimental. While no one argues against the single species philosophy in principle, numer• ous practical difficulties are evident (Huffaker et aI., 1971; Stehr, 1973). Finding and preranking every possible candidate for introduction appears to be unrealis• tic, especially since a definite set of criteria for such an undertaking has yet to be developed. In addition, researchers rarely have either the time or the funds avail• able to carry out such a program. Multiple species advocates have argued since the time of Smith (1929) in favor of introducing every reasonable prospective natural enemy and letting them sort themselves out. Among the supporters of this strategy are Balch et al. (1958), Doutt and DeBach (1964), Huffaker and Kennett 66 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

(1966), and DeBach (1974), who feel that the potential for adversity in the introd• uction of several beneficial species at once is minimal, especially when weighed against its advantages. First of all, it is, at present, the only practical way of obtaining the "best" species, or combination of species, for pest regulation in the new habitat. It is unlikely that anyone beneficial species will be equally effective in all areas of the target pest's range, and the introduction of several species at localities representing all of the habitat extremes presents the greatest chance of establishing the "best" combination in each. While it is frequently the case that one introduced beneficial species is sufficient to regulate a pest at low population levels, it is sometimes necessary to add one or more species to achieve complete success (Quednau, 1970), and multiple introductions may be required. The so• called "sequence theory" suggests that, in some cases, a number of beneficial species, each one attacking a different life stage of the pest, may be required to achieve satisfactorily low pest densities (Howard and Fiske, 1911), and many workers believe that a diverse natural enemy complex provides stability and resiliency in pest regulation (Balch et al., 1958). Although the issue is still open to debate, biological control workers responsi• ble for introduction programs have generally accepted the multiple species con• cept as a useful working hypothesis. Most agree with the suggestion of DeBach (1972, 1974) that if an imported beneficial species displaces a fairly effective spe• cies already established, then the second one is even more efficient and will provide even better pest regulation. Thus, competing beneficial species may affect each other's individual efficiency, but their combined effect on host density is greater than either alone. Diamond (1973) has shown mathematically that most available population models support the multiple species philosophy. If this is true, then we need only to introduce potentially useful organisms into the pest community without extensive and detailed analysis of their potentialities. If the new species displaces one or more of the incumbent species, it will provide better pest suppression; if it fails to establish, no harm will be done. Of course we obtain as much information about each new species as possible, but practically speaking many successful programs have proceeded without detailed attempts to prerank the beneficial organisms introduced. As the science of biological insect pest suppression advances, such evaluation may become more commonplace, but, until the present, contemporaneous multiple species introductions have at least proven practical and safe. Multiple species introduction of beneficial organisms is closely allied to the principle known as Gause's Law, which states that different species occupying identical ecological niches (i.e. ecological homologues) cannot coexist indefinitely in the same habitat (Gause, 1934). The two species need not ever come in contact physically (e.g. predation or combat), but some critical resource, such as host or prey, must be subject to the same sort of utilization by both species. The species which is intrinsically better able to utilize the contested resource will prevail, while the other is crowded out. This type of competitive displacement has been observed several times with introductions of exotic beneficial organisms. Perhaps the classic example is that involving three braconid parasitoid species introduced to Hawaii against the oriental fruit fly, D. dorsalis Hendel (van den Bosch and Haramoto, 1953). Two of the parasitoids, Biosteres (Opius) longicaudatus (Ash- Introducing Genetic Diversity 67 mead) and Biosteres vandenboschi (Fullaway), were introduced in 1948, and B. lon• gicaudatus increased rapidly in abundance until late 1949, when it was replaced as the dominant parasitoid by B. vandenboschi. In 1949, a third species, Biosteres oophilus (Fullaway), was established, and during 1950 it displaced B. vandenbos• chi. Each succeeding displacement produced increased total parasitization and lower fruit fly densities, and later studies indicate that B. oophilus has maintained its dominance while the other two species are present in only low numbers (Bess and Haramoto, 1958). In another similar case, dominant hymenopterous parasit• oids of the genus Aphytis attacking the California red scale were successively replaced twice by newly introduced more effective congeners (DeBach, 1966; DeBach et al., 1971). A more recent instance of the phenomenon was noted in Wisconsin, where an ichneumonid parasitoid, E. amictorius has displaced the torymid, Monodontomerus dentipes (Dalman), as the dominant parasitoid of the introduced pine sawfly, Diprion similis (Hartig) (Mertins and Coppel, 1968, 1974).

2.3.3.3 Introducing Genetic Diversity The success of biological insect pest suppression through the introduction of predators or parasitoids rests first on their ability to survive in the new environ• ment. Observed genetic variation within the regional population of exotic benefi• cial organisms has prompted a largely theoretical debate over whether introduced species have a better chance of survival when the colonized stock is genetically diverse or when it is homogeneous. Adequate empirical evidence is lacking on either side. The theory of population genetics indicates that genetic variability differs between the ecologically favorable center of distribution and the ecological mar• gins of a species (Dobzhansky et al., 1963). The larger breeding unit at the distri• butional center is more heterozygous apparently because more alleles are intro• duced into the population by mutation (Remington, 1968). Not only is the popu• lation more abundant, but more outbred and more stable. Smaller peripheral populations tend to have fewer alleles at each locus and are more inbred and homozygous. Arguing that the more heterogeneous central population contains a higher frequency of lethal genes, Remington (1968) suggested that beneficial organism stock should come from the ecological margins of distribution where there is little genetic diversity and lower genetic load. If very large numbers of individuals are released in a new environment the lethal mutations from the central population would be of little consequence, but small colonies might be difficult to establish. Lucas (1969) agrees with the postulated distribution of heterogeneity in a regional population, but differs in the conclusion he draws. Like Turner and Williamson (1968), Lucas feels that genetic load may be relatively unimportant in preventing the establishment of introduced beneficial organisms. Instead, he argues that introduced entomophages should be as genetically diverse as possible and come from the ecological center of distribution. This greater genetic variability com• bined with the process of natural selection should sort out the best suited geno• type for the new environment. In short, the hope of adaptation is more important than the fear oflethal genes, and maximum variability is most desirable. 68 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression

The current practice of multiple introductions of various geographic strains, races, or ecotypes, as advocated by Bartlett and van den Bosch (1964), Doutt and DeBach (1964), and DeBach (1974) is another way of approaching the problem as it was formulated and addressed by Lewontin (1965) and Whitten (1970). These authors suggest that the best strategy may be to release as many separate samples as possible, derived mainly from the ecological margins of distribution but includ• ing some from the center, in the hopes that at least one of the samples is already preadapted to the new environment. Sometimes the introduction of genetic diversity is a little less empirical. Two recent examples illustrate how an observed deficiency in an established beneficial organism may be overcome by seeking out and substituting a genetically superior strain. For example, Mesolieus tenthredinis Morley, an introduced ichneumonid parasitoid of the larch sawfly, Pristiphora erichsonii (Hartig), was initially a very efficient regulator of sawfly populations in Canada (McLeod et aI., 1962). In recent years a resistant strain of sawflies capable of encapsulating M esolieus eggs has been increasing in central Canada and escaping regulation. However, a reas• sessment of M. tenthredinus populations in Europe discovered a Bavarian strain exhibiting a genetically dominant capability to overcome encapsulation by the host (Turnock and Muldrew, 1971). Establishment ofthis strain in Canada should displace the inferior strain and restore the regulative abilities of the parasitoid population. Bartlett (1974) reported on efforts to improve cold-tolerance in the introduced coccinellid mealybug predator, C. montrouzieri Mulsant. The original stock of C. montrouzieri came to California from mild climatic regions of Aus• tralia in 1891, and these have had to be maintained in the insectary and reesta• blished yearly in the spring in all but the warmest areas of the State. However, a new cold-tolerant stock has now been obtained from two colder areas of Austral• ia, propagated, and colonized in California, and gives promise of permanent establishment.

2.3.3.4 Host-Specificity and the Relative Value of Predators and Parasitoids Despite some dissension (Thompson, 1929, 1951b), the general feeling among biological control workers is that monophagous, or narrowly oligophagous ento• mophages present the greatest promise for use in pest suppression (Doutt and DeBach, 1964). The record of successful instances of biological insect pest sup• pression tends to support this contention (DeBach, 1974), and the implication is that a highly specific entomophage is biologically well-adapted to its host/prey and, hence, most likely to demonstrate a directly density-dependent and regula• tive relationship with the pest population. On the other hand, a polyphagous species is less directly tied to the density variations of a particular host/prey and less likely to playa regulative role. A general feeder does have some advantages over a monophagous species, however, which may make it a desirable prospect for pest suppression. For example, adaptive host/prey specificity is usually corre• lated with reduced environmental adaptability. Thus, if the pest species is subject to periodic population collapse caused by other factors, a specific entomophage will suffer similarily, while a polyphagous species may maintain its numbers on other hosts (Stehr, 1973). The superior environmental adaptive ability of a general Host-Specificity and the Relative Value of Predators and Parasitoids 69 feeder also permits it to increase its effective spatial distribution more rapidly by using alternate hosts/prey, especially in situations where the target pest is discon• tinuously distributed. On balance, it seems that a high degree of specificity has proven desirable in past programs and will remain an important attribute in most future importations of beneficial organisms, but in some cases oligophagous or polyphagous species may be advantageously used for biological pest suppression. Consideration of the relative merits of monophagy and polyphagy leads us to a discussion of the comparative value of parasitoids and insect predators in biological insect pest suppression. This is because of the long held belief that parasitoids tend to be more monophagous than predators, which tend toward polyphagy. One basic characteristic difference useful in distinguishing between parasitic and predaceous insects is the fact that predators consume more than one host (= prey) in order to reach maturity, whereas parasitoids develop completely at the expense of one host individual. The belief that predators are more polypha• gous than parasitoids probably stems from this fact, because the highly mobile individual predator can frequently be observed moving from one host to another, sometimes of a different species. On the other hand, an individual immature parasitoid is permanently, and apparently more intimately, associated with a single host species. In parasitic insects, however, mobility is a function of the adult stage, and, in fact, unobserved oviposition could occur on or in a large number of host species. So at the species level a parasitoid might easily attack as wide a variety of hosts/prey as a predator. In point of fact, there appears to be little difference in the specificity of parasitoids and predators (Thompson, 1929). As parasitoid biologies become better known, fewer and fewer species remain in the ranks of the strictly monophagous; conversely, many insect predators can be shown to be at least relatively restrictive in their selection of prey (Thompson, 1929,1951 b). The most important mutual similarities between parasitoids and insect preda• tors are that their attacks are practically always lethal to the host/prey and that both groups tend to behave in a density-dependent manner. We have suggested that a rapid, strong, and positive numerical density response is the most impor• tant attribute of a successful agent of pest mortality (see 2.3.1.3), and both parasitoids and insect predators appear to be capable of meeting this require• ment. A number of characteristics are contributory to the density-dependent response we seek. Of these, we have already discussed host/prey-specificity and concluded that parasitoids and predators are comparable in this regard. Other important contributing characteristics are reproductive potential, searching ca• pacity, and dispersal ability. For each of these attributes there appear to be offsetting adaptations favoring either parasitoid or predator, such that in no case can we generalize that one group is superior to the other. For example, there are certain parasitic insects, such as acrocerid and some tachinid flies, eucharitid wasps, and the strepsipterans, which produce immense numbers of offspring. The way in which these offspring find a host, however, is very wasteful, and actual survival to adults of the following generation is rela• tively small. Although nothing comparable occurs amongst the insect predators, their actual reproductive capabilities as a group compare favorably with those of the parasitoids. The searching capacity of the two groups may be likewis~ com- 70 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression pared. In the parasitoids, host finding is normally accomplished by the highly motile adult female. Predators are usually active in seeking prey throughout their lives; the immature stages search for prey to feed upon, and the adults do so also in addition to seeking oviposition sites near appropriate prey species. Individual predators find and destroy a number of prey each, whereas individual parasitoids kill one or only part of one host (for gregarious species) in their development. This seeming advantage for predators may be offset by the fact that a parasitoid species should be able to survive at lower host density, at one host per immature parasi• toid, than a predator which requires a greater number of prey per individual in a given area for its development. The dispersal abilities of parasitoids and predators appear to be about equal, with all stages of the predators moving about, while dispersal of parasitoids occurs in the very motile adult stage. The highly contrasting and variable life strategies of parasitoids and insect predators as heterogeneous groups make it very difficult to theoretically assess their relative value as agents for biological insect pest suppression. We must still rely upon actual comparative introductions and field evaluations on a case by case basis (Thompson, 1929; Doutt and DeBach, 1964). It appears that both groups include species which are capable of effecting the results we seek. A num• ber of authors have pointed out the fact that insect predators have not received the attention due to them (Thompson, 1929; Doutt and DeBach, 1964; Sailer, 1971). Evidence in support of this contention comes from a number of published sum• maries which compare the number of successful cases of biological pest suppres• sion based on the use of parasitoids and predators. Clausen (1956) reported that of 95 entomophagous insects imported and established in the United States, 81 were parasitoids. Sweetman (1958) found that of 103 successful entomophages used against insect pests worldwide, 75 were paras ito ids. DeBach's (1964 b) esti• mate showed that 18 of 24 introduction programs judged to be complete successes involved parasitoids. McGugan and Coppel (1962) found that only one of 12 beneficial species released and established against Canadian forest insect pests was a predator. Parasitoids appear to hold the edge in utility in every case, but the statistics may well represent the preferences of entomologists more than they do the relative merits of parasitoids and predators. Thus, of all attempts listed by DeBach (1964 b), 129 involved parasitoids, 30 involved predators, and 3 a combi• nation of both; on a comparative percentage basis we see that, although only 20% of the attempts involved predators, 25% of the complete successes were based on their use. A possible explanation for the traditional prejudice in favor of parasi• toid introduction may well involve the relative difficulty of apprehending preda• tors for importation. As pointed out by Thompson (1929), whereas the chances of finding a predator in the act of devouring its prey might be less than one in one hundred for an observation lasting ten minutes, one might easily collect 100 host larvae in ten minutes time, and rear a number of parasitoids from them, no matter at what moment they were collected and when they were parasitized.

2.3.3.5 Functional and Numerical Response The intimate association between predators and their prey or parasitoids and their hosts means that population density changes in one group may well effect Functional and Numerical Response 71 complementary changes in the other group. We have emphasized the belief that pest population suppression may be accomplished by somehow increasing the numbers or effectiveness of the natural or introduced enemies associated with it. Although we are most interested in this type of relationship, it is also instructive to consider the effects of a changing pest density on the behavior and size of natural enemy populations. The number of pest insects destroyed by their associated natural enemies is dependent upon two separate but related elements: the number of parasitoids or predators present and the number of pest insects killed per entomophage. Increas• ing pest insect densities can affect either of these elements as discussed by Solo• mon (1949). Entomophagous insects may respond to increased host/prey density by increasing their own numbers, the so-called "numerical" response; or they may respond by increasing the number of hosts/prey that each individual destroys, the so-called "functional" response; or they may do both. Functional responses are the more basic and are rarely responsible by them• selves for pest population regulation (Huffaker et aI., 1971). They are generated by ethological and physiological processes within the entomophage itself and occur essentially on a short-term within generation basis. According to Holling (1959, 1966), a successful functional response is measured in terms of food consumption and may be dependent upon the following factors: rate of searching, length of time the prey/host is exposed to attack, handling time, hunger, development of a specific searching image (i.e. learning by the entomophage or inhibition by the pest insect), and various components of competition between entomophages at• tempting to more fully utilize the available pest insect population. Increased utilization of a pest which is increasing in density can occur in monophagous, oligophagous, or polyphagous entomophages, although it is least likely in the latter because the particular pest species may form only a small part of the normal diet of the entomophage. Nevertheless, more frequent encounters and learning ability may stimulate a polyphagous nat.ural enemy to at least supplant part of its diet with the readily available pest species. Numerical responses of entomophagous parasitoids and predators are usually of more interest to us than functional responses because they are most often responsible for suppressing pest populations (Huffaker et ai., 1971). This is illus• trated by the fact that introduced entomophagous insects generally require at least three generations of reproductive increase before their effect on a target pest population becomes noticeable. Overall, however, both response types interact, with the numerical response usually deriving from a preceding functional re• sponse. Thus, an increasing pest population stimulates the functional responses of increased attack and consumption by locally present entomophages. The in• creased utilization of a larger food supply tends to bring about two components of the numerical response: first, a direct and rapid improvement in entomophage survival and secondly, a subsequent increase in the effective reproductive rate (DeBach and Smith, 1941). A third component of the numerical response is a short-term and rapid increase in the local population of natural enemies due to immigration from surrounding areas where food is not as plentiful. The summa• tive effect of the three components of numerical response is to rapidly and perma• nently increase the number of beneficial organisms present in accordance with 72 Historical, Theoretical, and Philosophical Bases of Biological Insect Pest Suppression increased host/prey availability. Of course, as the local density of a pest insect decreases (perhaps due to the activities of its natural enemies), the components of numerical response may take on the negative characteristics of emigration, re• duced fertility, and lower survival because of a lower availability of hosts/prey per individual; a decreasing natural enemy population will result. The study of such feedback responses between pest and natural enemy is one facet of the field of population dynamics (Chap. 2.2). Many authors have dealt with the subject on a theoretical or mathematical basis (Bombosch, 1963; Morris, 1963b; Holling, 1966; van Emden, 1966; Mukerji and LeRoux, 1969; Griffiths and Holling, 1969; Scopes, 1969b; Tamaki et al., 1974), but, as suggested by Royama (1971), who reviewed and criticized the state of affairs, we are still at the relatively primitive stage of descriptive ecology, and there is still much to be learned before we can adequately understand and use these complicated biologi• cal principles to our advantage.