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Introduction to symposium on biological control
Agriculture, Ecosystems and Environment, 15 (1986) 85--93
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Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
INTRODUCTION TO SYMPOSIUM ON BIOLOGICAL C O N T R O L
C.B. H U F F A K E R
Division of Biological Control, Department of Entomological Sciences, University of California, Berkeley, CA (U.S.A.) (Accepted for publication 14 March 1985)
I would like to discuss some developments and programs of biological control which point to new possibilities or increased attention to old ones. I believe the introduction of natural enemies into new areas which a pest has invaded will remain a fruitful endeavor; yet even here more attention to modern taxonomic methods for identifying sibling species and strains, better climatic fits, and characteristics most likely to prove beneficial should produce continuing successes. Beyond continuing classical introd "ctions we need to develop more ways of using indigenous natural enemies. Let me say emphatically that we need also to protect the uniqueness of our discipline from the lumpers who wish to include all biological forms as "biological control". I would note that this lumping has served wrongly to indict our area by association (with some failures of such methods as use of hormones and sterile male releases). Biological control of insects is rather generally considered to include only the use of parasitoids, predators and pathogens, while "antagonists" is a related term in the biological control of plant pathogens. The unique role of such natural enemies in reducing their hosts' populations is a phenomenon of host--enemy population interaction. Use of hormones, or sterile or genetically deranged insects of the pest species itself, is clearly not the same. At the time this paper was written The Special Issue of Agriculture, Ecosystems and Environment, "Biological Control" (Vol. 10, No. 2, 1983) had not appeared. That excellent treatment coincides precisely in scope and in principle with what I have considered here as appropriate to the discipline of biological control. The premise on which biological control rests is that in certain circumstances many populations are held at low densities by their by parasitoids, predators, pathogens, and other "antagonists". For many species that are pests or potential pests of crops, these natural enemies provide ample crop protection. This premise is simply one aspect of the "balance of nature", which implies that populations are restricted in numbers; that because of their increase in density they use up resources, defile their habitat or abodes or generate other increased intensity of inimical factors, such as predators, parasites, and pathogens. Classical biological control is, then, an effort to
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86 establish in a new area, a biological control link existing in the native home area, by introducing an effective natural enemy {or enemies) from the home area of a pest species into another region the pest has invaded. The role of predators and parasitoids in producing a regulating role, as implied by the term "balance of nature", has received much experimental and theoretical study in both laboratory and field (see, e.g., DeBach and Bartlett, 1964; DeBach, 1974; Huffaker and Messenger, 1976; Huffaker et al., 1976; Hassell, 1978; Luck, 1985; and refs. cited in these papers), and also extensive "experimentation" over broad geographic regions by the introduction of such agents into environments lacking in them, as noted elsewhere in these Congress proceedings (cf., e.g., Laing and Hamai, 1976; Harper, 1977; Clausen, 1978; and previous citations). The roles of pathogens and other antagonists, or related organismal interactions, have been studied less in these respects, but recent years have seen a major acceleration of such work (cf. Burges and Hussey, 1971; Baker and Cook, 1974; Snyder et al., 1976; Kommedahl, 1981). The role of predators and parasitoids in the applied biological control of insect pests was, as is so well known, first spectacularly demonstrated by the introduction of Rodolia cardinalis (Mulsant) into California in 1888 to control c o t t o n y cushion scale, Icerya purchasi Mask., which so threatened the y o u n g citrus industry. The success was so great as to herald worldwide efforts of a similar nature. The control in California has remained virtually complete to this day, despite heavy use of various insecticides. Following this spectacular success a worldwide traffic in exploration and importation of biological control agents developed. This was not restricted to its uses against insects, b u t also against weeds (e.g., Hagen and Franz, 1973; Simmonds et al., 1976). Classical biological control has resulted in some 140 or more cases of substantial or complete success with given insect pests and some 40 cases with weeds. The impact of predators and parasitoids has thus been broadly demonstrated via introductions. However, perhaps even more significant, the role of native parasitoids and predators in holding native potential pests under control was spectacularly demonstrated with the wide use of DDT and other insecticides in the late 1940's and early 1950's. Just as DDT, when used on citrus, killed Rodolia and occasioned explosive resurgences of the c o t t o n y cushion scale, the use of DDT and various materials interfered with natural enemies so as to result in explosions of many alien, and also native, species that had formerly been of relatively little or no consequence to various crops. As many have noted, this naturally occurring biological control exists all around us; without it our pest problems would be much greater. Thus, the disturbances by pesticides simply uncovered this natural control and created many "induced pests" {DeBach, 1974, and many others). Integrated control is often concerned with correction of these induced pest problems, and of course with pesticide-resistant strains. Examples of such induced pests were seen in the build-up of tetranychid
87 mites throughout the world (Porter, 1947; also, see reviews by McMurtry et al., 1970 and Huffaker et al., 1970), bollworms and budworms in cotton (Adkisson, 1971), bagworms in Malaysia (Wood, 1971), cyclamen mites in strawberries (Huffaker and Kennett, 1956), and many others (see Ripper, 1956}. The notorious, recent example is the tobacco budworm, Heliothis virescens (Fabricius), in areas of Texas, Mexico (Adkisson, 1971) and California (Smith and Reynolds, 1977). The striking success with the purposeful introduction of a pathogen against rhinoceros beetles (in this case using a virus) in the South Pacific is a landmark example (Bedford, 1980; Caltagirone, 1981) and is covered by Dr. Bedford in this symposium. It is upon this solid empirical base that applied biological control rests. At every stage in its development, funds to support it and enthusiasm to pursue it have derived from some new, surprising or spectacular practical success.
The theory of biological control, an ecological concept, goes well b e y o n d the theory of predator--prey (or host--parasite) interactions as a mathematical abstraction, as though such interactions occur without any intrusions from factors external to the interaction itself. Yet even such abstract theoretical studies furnish certain insights. The usual theoretical models of predator--prey (host--parasite) interactions deal with a single hypothetical, strictly host- or prey-specific predator or parasite species. Such population modeling has involved a pair of equations, one for the predator (or parasite) and one for the prey (or host). Only the predator or parasitoid species population is conceived as being resource (prey) limited; the prey (host) is limited by the predator (parasitoid) population linked with it in a completely reciprocal interaction. While even Volterra (1927) and some later (e.g., May, 1981) modelers also employed a logistictype of density-dependent resource restriction on a prey population having a dominant restriction by predators (parasitoids), and other workers (see Hassell, 1978) have introduced density-dependent stabilizing behavior of the predators, these models have still been based on the Lotka--Volterra or Nicholson--Bailey basic formulations. It is of interest that now a new approach to modeling host--parasite and predator--prey interactions (a m e t h o d more appropriate to field populations} has been explored by A.P. Gutierrez and associates in our Division of Biological Control at Berkeley. This method, at its basic level, assumes that predator population growth has a density-dependent response to the amount of resource (prey) available per capita predator population. This per capita resource availability is, in an elementary sense, the same as the notion of the supply/demand ratio used so successfully by Gutierrez and Baumgaertner (1984) to incorporate physiology and behavior into their predator--prey models. Predator demand will depend on the size of an organism, its age, its level of hunger, which may be a function of the number of day-degrees that have elapsed since its last meal, and on various other
88 physiological parameters. An important feature of this approach is that it unifies growth concepts at all trophic levels, and allows multiple trophiclevel models to be put together in a consistent manner (cf. Getz, 1985). Of recent interest is the demonstration that an herbivorous insect can become so well adapted to its aquatic plant host as to serve as an efficient regulator and control agent. Thus, the beetle Agasicles hygrophila, and the moth Vogtia malloi Past., introduced from Argentina to control alligator weed in the southeastern U.S., has proved to be highly adapted to this emergent aquatic, and produced savings of some US $40 000 per year in control operations by the U.S. Army Corps of Engineers alone. Very recently, the tiny beetle Cyrtobagous salvinia has similarly cleared Lake Moondara in Australia of the pest aquatic fern Salvinia molesta ( R o o m et al., 1981). Then, too, a complex of natural enemies may be more effective than the best one alone. Firstly, the complex of two parasitoids and a Borrelina virus has combined to produce striking, continuing biological control at very low endemic densities of the European spruce sawfly Diprion hercyniae Hartig in the Maritime provinces of Canada (Balch and Bird, 1944; Neilson and Morris, 1964; Neilson et al., 1971). The outbreak was brought down initially by the virus, whereas the subsequent low endemic densities were considered to be due mostly to the parasitoids, Drino bohemica Mesnil and Exenterus sp. Now it seems that the parasites may spread the virus at a host density t o o low to generate virus maintenance and full effectiveness in the absence of the parasites. Another example where two natural enemies are more effective, even in a given locale, than the " b e s t " one alone, is seen in the control of parlatoria scale, Parlatoria oleae (Colvee), in California by Aphytis paramaculicornis Masi and Coccophagoides utilis D o u t t (See Huffaker and Kennett, 1966). Phenomenal control is achieved by the two species even though the most efficient species, A. paramaculicornis, when present alone is not satisfactory in some locations and some years, and C. utilis when present alone fails entirely, the pest slowly regaining devastating abundance. It has long been recognized that sibling species or ecotypes of a species may exist over a broad heterogeneous distribution area, and that each sibling or e c o t y p e is especially adapted to the physical and biological conditions of its area. Introduction of a complex of types throughout such regions thus offers a better o p p o r t u n i t y to satisfy the needs of all the pest-infested areas. Exploration efforts are generally but by no means always concentrated in the home regions of the pest species most climatically similar to the target area. This feature was stressed by Clausen (1936) and has since been clearly rewarding. Flint (1979) notes that the literature contains a number of examples wherein introductions of given parasitoid species failed in a given area, b u t where a second introduction of a different climatic ecotype of the same, or a sibling, species was made, good biological control resulted; in Australia, for example, Trissolcus basalis (Wollaston) introduced against Nezara viridula L. (Ratcliffe, 1965); in British Columbia, Bigonocheta spinipennis Meigen,
89 against Forficula auricularia L. (McLeod, 1954); in California, Aphytis paramaculicornis (Masi) against Parlatoria oleae (Colv~e) (Huffaker et al., 1962); and Trioxys pallidus {Hal.) against the walnut aphid, Chromaphis juglandicola (Kalt.) (van den Bosch et al., 1979). Thus, general comparisons of the Iranian climate to California's interior valleys led the late R o b e r t van den Bosch to concentrate the search for parasitoids of alfalfa weevils, walnut aphids and some other pests in Iran. For the walnut aphid, T. pallidus had previously been introduced (in 1959) from France to California. It established and'spread rapidly in southern California but n o t in the north or central interior valley. Van den Bosch then imported this species from Iran and it became quickly established in all of California's walnut-growing areas and has resulted in complete biological control (Nowierski, 1979, van den Bosch et al., 1979), except when it is decimated by pesticides used against other pests. Besides introductions, there are many ways by which resident natural enemies may be conserved and/or augmented (see Ridgway and Vinson, 1977). As above, they can be conserved simply by stopping unnecessary use of pesticides inimical to them or their hosts, or by preserving habitats or subsidiary natural foods they require. Their conservation and augmentation can also be assisted by various ways of augmenting their numbers or improving environmental features favorable to them. Mass production and release of Trichogramma for the control of a wide variety of insects is widely practiced in the U.S.S.R., China, Mexico and some countries in South America, sometimes with success and sometimes failure. The effectiveness of many of these releases has not been closely evaluated, b u t enough data exist to indicate the real effectiveness of some programs. U.S.S.R. and Chinese workers consider a main reason for failures to be that the species and strains of Trichogramma are differentially adapted to a particular pest species and/or host habitat and that the wrong ones have t o o often been used. The most interesting development I know of is China's current, successful program of rearing Trichogramma in non-host, artificial eggs. The artificial host material {either a pure chemically defined diet or one employing, among other things, chicken eggs) is encapsulated in tiny egg-like spheres coated with wax and plastic blown out from an aspirator-type machine. The "eggs" are caught in a gauze apron. The possibilities of yearly release each spring of a natural enemy that cann o t overwinter in a given area is suggested by the highly successful spring releases of Pediobius epilachinae against the Mexican bean beetle, Epilachna varivestis Mulsant, in some southern states of U . S . A . R . I . Sailer {see Huffaker, 1981) has reported phenomenal success, and the costs of such a program, in some situations at any rate, seem most promising. I should also note the possible e m p l o y m e n t of behavioral chemicals to augment the effectiveness of parasitoids and predators, which Dr. Vinson will cover in this symposium (see also Nordlund et al., 1981). Detailed
90 genetical improvement of a natural enemy has been demonstrated for a phytoseiid mite, and this will be covered by Dr. Hoy. Releases of a pest itself so as to carry a natural enemy over a period of absence of the host or to pre-establish the natural enemy at an early time of crop growth has been tested. Huffaker and Kennett (1956) demonstrated its potential feasibility for cyclamen mite control on strawberries but the technique was not adopted by growers. Likewise, Parker (1971) obtained good control of Piereis rapae L. in Missouri from field releases of small numbers of the pest butterflies during the critical period, combined with releases of both Trichogramma evanescens Westw. and Apanteles rubecula Marsh. Again, the m e t h o d has not been adopted by growers. In China, however, this procedure is accepted in purple lac culture (Guyer, 1977). A moth caterpillar, Eublema amabilis Moore, eats the lac and can cause serious losses. The parasite Bracon greeni Ashmead is released for its control. There is a season in the year, however, when the parasite population has t o o few hosts to sustain itself, so light infestations of the pest moth are initiated on the trees to bridge the gap. Integrated pest management (IPM), as used in glasshouses wherein the pest is introduced first, is another example of pest introduction to establish a beneficial pest--natural enemy interaction (see below). Also, as will be discussed by Dr. Garcia and others, substantial research progress has been made in the discovery and development of a strain of Bacillus thuringiensis for use in mosquito and blackfly control. Then too, biological control and pest-resistant varieties serve as the central feature of most integrated control (IPM) programs, with these methods integrated closely with the selective use of pesticides. Most programs for developing integrated control, in fact, have involved restoration of biological control that has been disrupted by misuse of chemicals. Many also involve pests that have developed a high resistance to the materials used against them. Spider mites in glasshouses in the U.K. developed resistance to acaricides at an early stage. This led H.N. Hussey and associates to explore the possibilities of using predatory mites, Phytoseiulus persimilis Athias-Henriot, to control them, initially on cucumbers. This led to a program of IPM for a whole complex of glasshousepests. Dr. H.D. Burges, who is here, may be contacted concerning this. The greenhouse whitefly was known to be heavily parasitized by Encarsia formosa Gahan. The apid Myzus persicae (Sulzer) also had become a major pest in glasshouses and it too is sometimes effectively parasitized. Careful attention to the biologies of these hosts and natural enemies, glasshouse crop and natural enemy culture procedures, and glasshouse temperatures, gradually led to methods by which each of these pests can largely be controlled by releases of natural enemies, with only minimal, carefully programmed use of chemicals for other pests. Currently, the m e t h o d is rather c o m m o n l y used in the U.K. (Hussey and Scopes, 1977), the Netherlands (van Lenteren et al., 1980 and Finland (Markkula, 1980), and is being explored in the U.S.S.R. (Beglyarov, 1981). Lastly, a short-season IPM c o t t o n production system for South Texas has
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been developed to avoid prolonged exposure of the crop to boll weevils and the crop is harvested early so as greatly to reduce overwintering boll weevils; this is combined with chemical treatments for weevils destined to overwinter ("diapause" treatments); the weevil population is thus slow to develop the following season; hence, treatments in the summer can be delayed so that natural enemies of Heliothis spp. can keep those pests under control. In conclusion, I hope that these necessarily limited comments will serve to introduce the area of biological control. I would add that as either biological or integrated control advances, so does the other. They should not, however, be equated, as each would thereby lose some of its objectivity.
REFERENCES Adkisson, P.L., 1971. Objective uses of insecticides in agriculture. In: J. E. Swift (Editor), Agricultural Chemicals -- Harmony or Discord for Food, People, Environment. Division of Agricultural Sciences, University of California, pp. 43--51. Baker, K.F. and Cook, R.J., 1974. Biological Control of Plant Pathogens. Freeman and Co., San Francisco. Balch, R.E. and Bird, F.T., 1944. A disease of the European spruce sawfly, Gilpinia hercyniae (Htg.), and its place in natural control. Sci. Agric. (Ottawa), 25: 65--80. Bedford, G.O., 1980. Biology, ecology, and control of palm rhinoceros beetles. Annu. Rev. Entomol., 25: 309--339. Beglyarov, G.A., 1981. Advances in, and outlook for development of biological control to protect plants under glass in the U.S.S.R. In: Proc. Joint American--Soviet Conf. on Use of Beneficial Organisms in the Control of Crop Pests. Entomol. Soc. Am., College Park, MD, pp. 36--67. Burges, H.D. and Hussey, N.W. (Editors), 1971. Microbial Control of Insects and Mites. Academic Press, London. Caltagirone, L.E., 1981. Landmark examples in classical biological control. Annu. Rev. Entomol., 26: 213--232. Clausen, C.P., 1936. Insect parasitism and biological control. J. Econ. Entomol., 44: 1--9. Clausen, C.P. (Editor), 1978. Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. USDA Agriculture Handbook 480. DeBach, P., 1974. Biological Control by Natural Enemies. Cambridge University Press, Cambridge. DeBach, P. and Bartlett, B.R., 1964. Methods of colonization, recovery and evaluation. In: P. DeBach (Editor), Biological Control of Insect Pests and Weeds. Chapman and Hall, London, pp. 402--426. Flint, M.L., 1979. Geographic variation in Trioxys complanatus, a parasite of the spotted alfalfa aphid. Ph.D. Dissertation. University of California, Berkeley. Getz, W.M., 1985. Population dynamica: a per capita resource approach. J. Theor. Biol., in press. Gutierrez, A.P. and Baumgaertner, J.U., 1984. Multitrophie models of predator--prey energetics. II. A realistic model of plant--herbivore--parasitic--predator interactions. Can. Entomol., 116: 933--949. Guyer, G.E. (Delegation Chairman), 1977. Insect control in the People's Republic of China. Committee on Scholarly Communication with the People's Republic of China. National Academy of Science, Washington, DC. Hagen, K.S. and Franz, J.M., 1973. A history of biological control. In: R.F. Smith, T.E. Mittler and C.N. Smith (Editors), A History of Entomology, Annu. Rev. Entomol., Palo Alto, Ca., pp. 433--476.
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Harper, J.L., 1977. Population Biology for Plants. Academic Press, New York. Hassell, M.P., 1978. The Dynamics of Arthropod Predator--Prey System. Princeton University Press, Princeton, NJ. Huffaker, C.B., 1981. Prospects for development of biological control methods for crop protection in the U.S.A. In: Proc. Joint American--Soviet Conf. on the Use of Beneficial Organisms in the Control of Crop Pests. Entomol. Soc. Am., College Park, MD, pp. 14--20. Huffaker, C.B. and Kennett, C.E., 1956. Experimental studies on predation. I. Predation and cyclamen mite populations on strawberries in California. Hilgardia, 26: 191--222. Huffaker, C.B. and Kennett, C.E., 1966. Studies of two parasites of olive scale, Parlatoria oleae (Colv~e). IV. Biological Control of Parlatoria oleae (Colv~e) through the compensatory action of two introduced parasites. Hilgardia, 37 : 283--335. Huffaker, C.B. and Messenger, P.S. (Editors), 1976. Theory and Practice of Biological Control. Academic Press, New York. Huffaker, C.B., Kennett, C.E. and Finney, G.L., 1962. Biological control of olive scale, Parlatoria oleae (Colv6e) in California by imported Aphytis maculicornis (Masi) (Hymenoptera: Aphelinidae). Hilgardia, 32: 541--636. Huffaker, C.B., van de Vrie, M. and McMurtry, J.A., 1970. Ecology of tetranychid mites and their natural enemies: a review. II. Tetranychid populations and their possible control by predators: an evaluation. Hilgardia, 40: 391--458. Huffaker, C.B., Luck, R.F. and Messenger, P.S., 1976. The ecological basis of biological control. Proc. 15th Int. Congress on Entomology, Washington, DC, pp. 559--586. Hussey, N.W. and Scopes, N.E.A., 1977. The introduction of natural enemies for pest control in glasshouses: ecological considerations. In: R.L. Ridgeway and S.B. Vinson (Editors), Biological Control by Augmentation of Natural Enemies. Plenum Press, New York, pp. 349--377. Kommedahl, T. (Editor), 1981. Proc. Syrup., IX Int. Congress of Plant Protection, Washington, DC, 1979. Laing, J.E. and Hamai, J., 1976. Biological control of insects pests and weeds by imported parasites, predators and pathogens. In: C.B. Huffaker and P.S. Messenger (Editors), Theory and Practice of Biological Control. Academic Press, New York, Chap. 28. Luck, R.F., 1985. Principles of arthropod predation. In: C.B. Huffaker and R.L. Rabb (Editors), Ecological Entomology. Wiley, New York, Chap. 16. Markkula, M., 1980. Biological control of pests in glasshouses in Finland -- the situation today and in the future. Bull. O.I.L.B./S.R.O.P., 3 (3): 127--134. May, R.M., 1981. Models for two interacting populations. In: R.M. May (Editor), Theoretical Ecology: Principles and Applications. 2nd edn., Sinauer Associates, Sunderland, MA, pp. 78--104. McLeod, J.H., 1954. Statuses of some introduced parasites and their hosts in British Columbia. Proc. Entomol. Soc. Brit. Columbia, 50: 19--27. McMurtry, J.A., van de Vrie, M. and Huffaker, C.B., 1970. Ecology of tetranychid mites and their natural enemies: a review. I. Tetranychid enemies: their biological characters and the impact of spray practices. Hilgardia, 40: 331--390. Neilson, M.M. and Morris, R.F., 1964. The regulation of European spruce sawfly numbers in the Maritime Provinces of Canada from 1937 to 1963. Can. Entomol., 96: 773-794. Neilson, M.M., Martineau, R. and Rose, A.H., 1971. Diprion hercyniae (Hartig), European spruce sawfly (Hymenoptera: Diprionidae). Commonw. Biol. Control Tech. Commun., 4: 136--143. Nordlund, D.A., Jones, R.L. and Lewis, W.J. (Editors), 1981. Semiochemicals: their Role in Pest Control. Wiley, New York. Nowierski, R.M., 1979. The field ecology of the walnut aphid, Chromaphis juglandicola (Homoptera: Aphidae) and its introduced parasite Trioxys pallidus (Hymenoptera: Aphididae) a qualitative and quantitative assessment of population regulation. Ph.D. Dissertation, University of California, Berkeley.
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Parker, F.D., 1971. Management of pest populations by manipulating densities of both hosts and parasites through periodic releases. In: C.B. Huffaker (Editor), Biological Control. Plenum Press, New York, Chap. 16. Porter, B.A., 1947. Orchard insecticides. In: Yearbook of Agriculture, Washington, DC, pp. 659--662. Ratcliffe, F.N., 1965. Biological control. Aust. J. Sci., 28: 237--240. Ridgway, R.L. and Vinson, S.B. (Editors), 1977. Biological Control by Augmentation of Natural Enemies. Plenum Press, New York. Ripper, W.E., 1956. Effect of pesticides on balance of arthropod populations. Annu. Rev. Entomol., 1 : 403--438. Room, P.M., Harley, K.L.S., Forno, I.W. and Sands, D.P.A., 1981. Successful biological control of the floating weed salvini. Nature (London), 294 (5836): 78--80. Simmonds, F.J., Franz, J.M. and Sailer, R.I., 1976. History of biological control. In: C.B. Huffaker and P.S. Messenger (Editors), Theory and Practice of Biological Control. Academic Press, New York, Chap. 2. Smith, R.F. and Reynolds, H.T., 1977. Some economic implications of pesticide overuse in cotton. In: New Frontiers in Pest Management. Conf. Proc., Sacramento, CA, pp. 25--34. Snyder, W.C., Wallis, G.W. and Smith, S.N., 1976. Biological control of plant pathogens. In: C.B. Huffaker and P.S. Messenger (Editors), Theory and Practice of Biological Control. Academic Press, New York, pp. 521--539. Van den Bosch, R., Horn, R., Matteson, P., Frazer, B.D., Messenger, P.S. and David, C.S., 1979. Biological control of the walnut aphid in California: impact of the parasite, Trioxys pallidus. Hilgardia, 47: 1--13. Van Lenteren, J.C., Ramakers, P.M.J. and Woets, J., 1980. Integrated control of vegetable pests in greenhouses. In: Integrated Control of Insect Pests in the Netherlands, Pudoc, Wageningen, pp. 109--118. Volterra, V., 1927. Variazioni e fluttuazioni del numero d'individui in specie animali conviventi. Venezia, Premiate Officine Grafiche C. Ferrari (translated into English by F.M. Scudo and J.R. Ziegler, 1978. The Golden Age of Theoretical Ecology: 1923-1940. Springer-Verlag, Berlin, pp. 153--159). Wood, B.J., 1971. Development of integrated control programs for pests of tropical perennial crops in Malaysia. In: C.B. Huffaker (Editor), Biological Control. Plenum Press, New York, Chap. 19.
85
Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
INTRODUCTION TO SYMPOSIUM ON BIOLOGICAL C O N T R O L
C.B. H U F F A K E R
Division of Biological Control, Department of Entomological Sciences, University of California, Berkeley, CA (U.S.A.) (Accepted for publication 14 March 1985)
I would like to discuss some developments and programs of biological control which point to new possibilities or increased attention to old ones. I believe the introduction of natural enemies into new areas which a pest has invaded will remain a fruitful endeavor; yet even here more attention to modern taxonomic methods for identifying sibling species and strains, better climatic fits, and characteristics most likely to prove beneficial should produce continuing successes. Beyond continuing classical introd "ctions we need to develop more ways of using indigenous natural enemies. Let me say emphatically that we need also to protect the uniqueness of our discipline from the lumpers who wish to include all biological forms as "biological control". I would note that this lumping has served wrongly to indict our area by association (with some failures of such methods as use of hormones and sterile male releases). Biological control of insects is rather generally considered to include only the use of parasitoids, predators and pathogens, while "antagonists" is a related term in the biological control of plant pathogens. The unique role of such natural enemies in reducing their hosts' populations is a phenomenon of host--enemy population interaction. Use of hormones, or sterile or genetically deranged insects of the pest species itself, is clearly not the same. At the time this paper was written The Special Issue of Agriculture, Ecosystems and Environment, "Biological Control" (Vol. 10, No. 2, 1983) had not appeared. That excellent treatment coincides precisely in scope and in principle with what I have considered here as appropriate to the discipline of biological control. The premise on which biological control rests is that in certain circumstances many populations are held at low densities by their by parasitoids, predators, pathogens, and other "antagonists". For many species that are pests or potential pests of crops, these natural enemies provide ample crop protection. This premise is simply one aspect of the "balance of nature", which implies that populations are restricted in numbers; that because of their increase in density they use up resources, defile their habitat or abodes or generate other increased intensity of inimical factors, such as predators, parasites, and pathogens. Classical biological control is, then, an effort to
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86 establish in a new area, a biological control link existing in the native home area, by introducing an effective natural enemy {or enemies) from the home area of a pest species into another region the pest has invaded. The role of predators and parasitoids in producing a regulating role, as implied by the term "balance of nature", has received much experimental and theoretical study in both laboratory and field (see, e.g., DeBach and Bartlett, 1964; DeBach, 1974; Huffaker and Messenger, 1976; Huffaker et al., 1976; Hassell, 1978; Luck, 1985; and refs. cited in these papers), and also extensive "experimentation" over broad geographic regions by the introduction of such agents into environments lacking in them, as noted elsewhere in these Congress proceedings (cf., e.g., Laing and Hamai, 1976; Harper, 1977; Clausen, 1978; and previous citations). The roles of pathogens and other antagonists, or related organismal interactions, have been studied less in these respects, but recent years have seen a major acceleration of such work (cf. Burges and Hussey, 1971; Baker and Cook, 1974; Snyder et al., 1976; Kommedahl, 1981). The role of predators and parasitoids in the applied biological control of insect pests was, as is so well known, first spectacularly demonstrated by the introduction of Rodolia cardinalis (Mulsant) into California in 1888 to control c o t t o n y cushion scale, Icerya purchasi Mask., which so threatened the y o u n g citrus industry. The success was so great as to herald worldwide efforts of a similar nature. The control in California has remained virtually complete to this day, despite heavy use of various insecticides. Following this spectacular success a worldwide traffic in exploration and importation of biological control agents developed. This was not restricted to its uses against insects, b u t also against weeds (e.g., Hagen and Franz, 1973; Simmonds et al., 1976). Classical biological control has resulted in some 140 or more cases of substantial or complete success with given insect pests and some 40 cases with weeds. The impact of predators and parasitoids has thus been broadly demonstrated via introductions. However, perhaps even more significant, the role of native parasitoids and predators in holding native potential pests under control was spectacularly demonstrated with the wide use of DDT and other insecticides in the late 1940's and early 1950's. Just as DDT, when used on citrus, killed Rodolia and occasioned explosive resurgences of the c o t t o n y cushion scale, the use of DDT and various materials interfered with natural enemies so as to result in explosions of many alien, and also native, species that had formerly been of relatively little or no consequence to various crops. As many have noted, this naturally occurring biological control exists all around us; without it our pest problems would be much greater. Thus, the disturbances by pesticides simply uncovered this natural control and created many "induced pests" {DeBach, 1974, and many others). Integrated control is often concerned with correction of these induced pest problems, and of course with pesticide-resistant strains. Examples of such induced pests were seen in the build-up of tetranychid
87 mites throughout the world (Porter, 1947; also, see reviews by McMurtry et al., 1970 and Huffaker et al., 1970), bollworms and budworms in cotton (Adkisson, 1971), bagworms in Malaysia (Wood, 1971), cyclamen mites in strawberries (Huffaker and Kennett, 1956), and many others (see Ripper, 1956}. The notorious, recent example is the tobacco budworm, Heliothis virescens (Fabricius), in areas of Texas, Mexico (Adkisson, 1971) and California (Smith and Reynolds, 1977). The striking success with the purposeful introduction of a pathogen against rhinoceros beetles (in this case using a virus) in the South Pacific is a landmark example (Bedford, 1980; Caltagirone, 1981) and is covered by Dr. Bedford in this symposium. It is upon this solid empirical base that applied biological control rests. At every stage in its development, funds to support it and enthusiasm to pursue it have derived from some new, surprising or spectacular practical success.
The theory of biological control, an ecological concept, goes well b e y o n d the theory of predator--prey (or host--parasite) interactions as a mathematical abstraction, as though such interactions occur without any intrusions from factors external to the interaction itself. Yet even such abstract theoretical studies furnish certain insights. The usual theoretical models of predator--prey (host--parasite) interactions deal with a single hypothetical, strictly host- or prey-specific predator or parasite species. Such population modeling has involved a pair of equations, one for the predator (or parasite) and one for the prey (or host). Only the predator or parasitoid species population is conceived as being resource (prey) limited; the prey (host) is limited by the predator (parasitoid) population linked with it in a completely reciprocal interaction. While even Volterra (1927) and some later (e.g., May, 1981) modelers also employed a logistictype of density-dependent resource restriction on a prey population having a dominant restriction by predators (parasitoids), and other workers (see Hassell, 1978) have introduced density-dependent stabilizing behavior of the predators, these models have still been based on the Lotka--Volterra or Nicholson--Bailey basic formulations. It is of interest that now a new approach to modeling host--parasite and predator--prey interactions (a m e t h o d more appropriate to field populations} has been explored by A.P. Gutierrez and associates in our Division of Biological Control at Berkeley. This method, at its basic level, assumes that predator population growth has a density-dependent response to the amount of resource (prey) available per capita predator population. This per capita resource availability is, in an elementary sense, the same as the notion of the supply/demand ratio used so successfully by Gutierrez and Baumgaertner (1984) to incorporate physiology and behavior into their predator--prey models. Predator demand will depend on the size of an organism, its age, its level of hunger, which may be a function of the number of day-degrees that have elapsed since its last meal, and on various other
88 physiological parameters. An important feature of this approach is that it unifies growth concepts at all trophic levels, and allows multiple trophiclevel models to be put together in a consistent manner (cf. Getz, 1985). Of recent interest is the demonstration that an herbivorous insect can become so well adapted to its aquatic plant host as to serve as an efficient regulator and control agent. Thus, the beetle Agasicles hygrophila, and the moth Vogtia malloi Past., introduced from Argentina to control alligator weed in the southeastern U.S., has proved to be highly adapted to this emergent aquatic, and produced savings of some US $40 000 per year in control operations by the U.S. Army Corps of Engineers alone. Very recently, the tiny beetle Cyrtobagous salvinia has similarly cleared Lake Moondara in Australia of the pest aquatic fern Salvinia molesta ( R o o m et al., 1981). Then, too, a complex of natural enemies may be more effective than the best one alone. Firstly, the complex of two parasitoids and a Borrelina virus has combined to produce striking, continuing biological control at very low endemic densities of the European spruce sawfly Diprion hercyniae Hartig in the Maritime provinces of Canada (Balch and Bird, 1944; Neilson and Morris, 1964; Neilson et al., 1971). The outbreak was brought down initially by the virus, whereas the subsequent low endemic densities were considered to be due mostly to the parasitoids, Drino bohemica Mesnil and Exenterus sp. Now it seems that the parasites may spread the virus at a host density t o o low to generate virus maintenance and full effectiveness in the absence of the parasites. Another example where two natural enemies are more effective, even in a given locale, than the " b e s t " one alone, is seen in the control of parlatoria scale, Parlatoria oleae (Colvee), in California by Aphytis paramaculicornis Masi and Coccophagoides utilis D o u t t (See Huffaker and Kennett, 1966). Phenomenal control is achieved by the two species even though the most efficient species, A. paramaculicornis, when present alone is not satisfactory in some locations and some years, and C. utilis when present alone fails entirely, the pest slowly regaining devastating abundance. It has long been recognized that sibling species or ecotypes of a species may exist over a broad heterogeneous distribution area, and that each sibling or e c o t y p e is especially adapted to the physical and biological conditions of its area. Introduction of a complex of types throughout such regions thus offers a better o p p o r t u n i t y to satisfy the needs of all the pest-infested areas. Exploration efforts are generally but by no means always concentrated in the home regions of the pest species most climatically similar to the target area. This feature was stressed by Clausen (1936) and has since been clearly rewarding. Flint (1979) notes that the literature contains a number of examples wherein introductions of given parasitoid species failed in a given area, b u t where a second introduction of a different climatic ecotype of the same, or a sibling, species was made, good biological control resulted; in Australia, for example, Trissolcus basalis (Wollaston) introduced against Nezara viridula L. (Ratcliffe, 1965); in British Columbia, Bigonocheta spinipennis Meigen,
89 against Forficula auricularia L. (McLeod, 1954); in California, Aphytis paramaculicornis (Masi) against Parlatoria oleae (Colv~e) (Huffaker et al., 1962); and Trioxys pallidus {Hal.) against the walnut aphid, Chromaphis juglandicola (Kalt.) (van den Bosch et al., 1979). Thus, general comparisons of the Iranian climate to California's interior valleys led the late R o b e r t van den Bosch to concentrate the search for parasitoids of alfalfa weevils, walnut aphids and some other pests in Iran. For the walnut aphid, T. pallidus had previously been introduced (in 1959) from France to California. It established and'spread rapidly in southern California but n o t in the north or central interior valley. Van den Bosch then imported this species from Iran and it became quickly established in all of California's walnut-growing areas and has resulted in complete biological control (Nowierski, 1979, van den Bosch et al., 1979), except when it is decimated by pesticides used against other pests. Besides introductions, there are many ways by which resident natural enemies may be conserved and/or augmented (see Ridgway and Vinson, 1977). As above, they can be conserved simply by stopping unnecessary use of pesticides inimical to them or their hosts, or by preserving habitats or subsidiary natural foods they require. Their conservation and augmentation can also be assisted by various ways of augmenting their numbers or improving environmental features favorable to them. Mass production and release of Trichogramma for the control of a wide variety of insects is widely practiced in the U.S.S.R., China, Mexico and some countries in South America, sometimes with success and sometimes failure. The effectiveness of many of these releases has not been closely evaluated, b u t enough data exist to indicate the real effectiveness of some programs. U.S.S.R. and Chinese workers consider a main reason for failures to be that the species and strains of Trichogramma are differentially adapted to a particular pest species and/or host habitat and that the wrong ones have t o o often been used. The most interesting development I know of is China's current, successful program of rearing Trichogramma in non-host, artificial eggs. The artificial host material {either a pure chemically defined diet or one employing, among other things, chicken eggs) is encapsulated in tiny egg-like spheres coated with wax and plastic blown out from an aspirator-type machine. The "eggs" are caught in a gauze apron. The possibilities of yearly release each spring of a natural enemy that cann o t overwinter in a given area is suggested by the highly successful spring releases of Pediobius epilachinae against the Mexican bean beetle, Epilachna varivestis Mulsant, in some southern states of U . S . A . R . I . Sailer {see Huffaker, 1981) has reported phenomenal success, and the costs of such a program, in some situations at any rate, seem most promising. I should also note the possible e m p l o y m e n t of behavioral chemicals to augment the effectiveness of parasitoids and predators, which Dr. Vinson will cover in this symposium (see also Nordlund et al., 1981). Detailed
90 genetical improvement of a natural enemy has been demonstrated for a phytoseiid mite, and this will be covered by Dr. Hoy. Releases of a pest itself so as to carry a natural enemy over a period of absence of the host or to pre-establish the natural enemy at an early time of crop growth has been tested. Huffaker and Kennett (1956) demonstrated its potential feasibility for cyclamen mite control on strawberries but the technique was not adopted by growers. Likewise, Parker (1971) obtained good control of Piereis rapae L. in Missouri from field releases of small numbers of the pest butterflies during the critical period, combined with releases of both Trichogramma evanescens Westw. and Apanteles rubecula Marsh. Again, the m e t h o d has not been adopted by growers. In China, however, this procedure is accepted in purple lac culture (Guyer, 1977). A moth caterpillar, Eublema amabilis Moore, eats the lac and can cause serious losses. The parasite Bracon greeni Ashmead is released for its control. There is a season in the year, however, when the parasite population has t o o few hosts to sustain itself, so light infestations of the pest moth are initiated on the trees to bridge the gap. Integrated pest management (IPM), as used in glasshouses wherein the pest is introduced first, is another example of pest introduction to establish a beneficial pest--natural enemy interaction (see below). Also, as will be discussed by Dr. Garcia and others, substantial research progress has been made in the discovery and development of a strain of Bacillus thuringiensis for use in mosquito and blackfly control. Then too, biological control and pest-resistant varieties serve as the central feature of most integrated control (IPM) programs, with these methods integrated closely with the selective use of pesticides. Most programs for developing integrated control, in fact, have involved restoration of biological control that has been disrupted by misuse of chemicals. Many also involve pests that have developed a high resistance to the materials used against them. Spider mites in glasshouses in the U.K. developed resistance to acaricides at an early stage. This led H.N. Hussey and associates to explore the possibilities of using predatory mites, Phytoseiulus persimilis Athias-Henriot, to control them, initially on cucumbers. This led to a program of IPM for a whole complex of glasshousepests. Dr. H.D. Burges, who is here, may be contacted concerning this. The greenhouse whitefly was known to be heavily parasitized by Encarsia formosa Gahan. The apid Myzus persicae (Sulzer) also had become a major pest in glasshouses and it too is sometimes effectively parasitized. Careful attention to the biologies of these hosts and natural enemies, glasshouse crop and natural enemy culture procedures, and glasshouse temperatures, gradually led to methods by which each of these pests can largely be controlled by releases of natural enemies, with only minimal, carefully programmed use of chemicals for other pests. Currently, the m e t h o d is rather c o m m o n l y used in the U.K. (Hussey and Scopes, 1977), the Netherlands (van Lenteren et al., 1980 and Finland (Markkula, 1980), and is being explored in the U.S.S.R. (Beglyarov, 1981). Lastly, a short-season IPM c o t t o n production system for South Texas has
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been developed to avoid prolonged exposure of the crop to boll weevils and the crop is harvested early so as greatly to reduce overwintering boll weevils; this is combined with chemical treatments for weevils destined to overwinter ("diapause" treatments); the weevil population is thus slow to develop the following season; hence, treatments in the summer can be delayed so that natural enemies of Heliothis spp. can keep those pests under control. In conclusion, I hope that these necessarily limited comments will serve to introduce the area of biological control. I would add that as either biological or integrated control advances, so does the other. They should not, however, be equated, as each would thereby lose some of its objectivity.
REFERENCES Adkisson, P.L., 1971. Objective uses of insecticides in agriculture. In: J. E. Swift (Editor), Agricultural Chemicals -- Harmony or Discord for Food, People, Environment. Division of Agricultural Sciences, University of California, pp. 43--51. Baker, K.F. and Cook, R.J., 1974. Biological Control of Plant Pathogens. Freeman and Co., San Francisco. Balch, R.E. and Bird, F.T., 1944. A disease of the European spruce sawfly, Gilpinia hercyniae (Htg.), and its place in natural control. Sci. Agric. (Ottawa), 25: 65--80. Bedford, G.O., 1980. Biology, ecology, and control of palm rhinoceros beetles. Annu. Rev. Entomol., 25: 309--339. Beglyarov, G.A., 1981. Advances in, and outlook for development of biological control to protect plants under glass in the U.S.S.R. In: Proc. Joint American--Soviet Conf. on Use of Beneficial Organisms in the Control of Crop Pests. Entomol. Soc. Am., College Park, MD, pp. 36--67. Burges, H.D. and Hussey, N.W. (Editors), 1971. Microbial Control of Insects and Mites. Academic Press, London. Caltagirone, L.E., 1981. Landmark examples in classical biological control. Annu. Rev. Entomol., 26: 213--232. Clausen, C.P., 1936. Insect parasitism and biological control. J. Econ. Entomol., 44: 1--9. Clausen, C.P. (Editor), 1978. Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. USDA Agriculture Handbook 480. DeBach, P., 1974. Biological Control by Natural Enemies. Cambridge University Press, Cambridge. DeBach, P. and Bartlett, B.R., 1964. Methods of colonization, recovery and evaluation. In: P. DeBach (Editor), Biological Control of Insect Pests and Weeds. Chapman and Hall, London, pp. 402--426. Flint, M.L., 1979. Geographic variation in Trioxys complanatus, a parasite of the spotted alfalfa aphid. Ph.D. Dissertation. University of California, Berkeley. Getz, W.M., 1985. Population dynamica: a per capita resource approach. J. Theor. Biol., in press. Gutierrez, A.P. and Baumgaertner, J.U., 1984. Multitrophie models of predator--prey energetics. II. A realistic model of plant--herbivore--parasitic--predator interactions. Can. Entomol., 116: 933--949. Guyer, G.E. (Delegation Chairman), 1977. Insect control in the People's Republic of China. Committee on Scholarly Communication with the People's Republic of China. National Academy of Science, Washington, DC. Hagen, K.S. and Franz, J.M., 1973. A history of biological control. In: R.F. Smith, T.E. Mittler and C.N. Smith (Editors), A History of Entomology, Annu. Rev. Entomol., Palo Alto, Ca., pp. 433--476.
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Harper, J.L., 1977. Population Biology for Plants. Academic Press, New York. Hassell, M.P., 1978. The Dynamics of Arthropod Predator--Prey System. Princeton University Press, Princeton, NJ. Huffaker, C.B., 1981. Prospects for development of biological control methods for crop protection in the U.S.A. In: Proc. Joint American--Soviet Conf. on the Use of Beneficial Organisms in the Control of Crop Pests. Entomol. Soc. Am., College Park, MD, pp. 14--20. Huffaker, C.B. and Kennett, C.E., 1956. Experimental studies on predation. I. Predation and cyclamen mite populations on strawberries in California. Hilgardia, 26: 191--222. Huffaker, C.B. and Kennett, C.E., 1966. Studies of two parasites of olive scale, Parlatoria oleae (Colv~e). IV. Biological Control of Parlatoria oleae (Colv~e) through the compensatory action of two introduced parasites. Hilgardia, 37 : 283--335. Huffaker, C.B. and Messenger, P.S. (Editors), 1976. Theory and Practice of Biological Control. Academic Press, New York. Huffaker, C.B., Kennett, C.E. and Finney, G.L., 1962. Biological control of olive scale, Parlatoria oleae (Colv6e) in California by imported Aphytis maculicornis (Masi) (Hymenoptera: Aphelinidae). Hilgardia, 32: 541--636. Huffaker, C.B., van de Vrie, M. and McMurtry, J.A., 1970. Ecology of tetranychid mites and their natural enemies: a review. II. Tetranychid populations and their possible control by predators: an evaluation. Hilgardia, 40: 391--458. Huffaker, C.B., Luck, R.F. and Messenger, P.S., 1976. The ecological basis of biological control. Proc. 15th Int. Congress on Entomology, Washington, DC, pp. 559--586. Hussey, N.W. and Scopes, N.E.A., 1977. The introduction of natural enemies for pest control in glasshouses: ecological considerations. In: R.L. Ridgeway and S.B. Vinson (Editors), Biological Control by Augmentation of Natural Enemies. Plenum Press, New York, pp. 349--377. Kommedahl, T. (Editor), 1981. Proc. Syrup., IX Int. Congress of Plant Protection, Washington, DC, 1979. Laing, J.E. and Hamai, J., 1976. Biological control of insects pests and weeds by imported parasites, predators and pathogens. In: C.B. Huffaker and P.S. Messenger (Editors), Theory and Practice of Biological Control. Academic Press, New York, Chap. 28. Luck, R.F., 1985. Principles of arthropod predation. In: C.B. Huffaker and R.L. Rabb (Editors), Ecological Entomology. Wiley, New York, Chap. 16. Markkula, M., 1980. Biological control of pests in glasshouses in Finland -- the situation today and in the future. Bull. O.I.L.B./S.R.O.P., 3 (3): 127--134. May, R.M., 1981. Models for two interacting populations. In: R.M. May (Editor), Theoretical Ecology: Principles and Applications. 2nd edn., Sinauer Associates, Sunderland, MA, pp. 78--104. McLeod, J.H., 1954. Statuses of some introduced parasites and their hosts in British Columbia. Proc. Entomol. Soc. Brit. Columbia, 50: 19--27. McMurtry, J.A., van de Vrie, M. and Huffaker, C.B., 1970. Ecology of tetranychid mites and their natural enemies: a review. I. Tetranychid enemies: their biological characters and the impact of spray practices. Hilgardia, 40: 331--390. Neilson, M.M. and Morris, R.F., 1964. The regulation of European spruce sawfly numbers in the Maritime Provinces of Canada from 1937 to 1963. Can. Entomol., 96: 773-794. Neilson, M.M., Martineau, R. and Rose, A.H., 1971. Diprion hercyniae (Hartig), European spruce sawfly (Hymenoptera: Diprionidae). Commonw. Biol. Control Tech. Commun., 4: 136--143. Nordlund, D.A., Jones, R.L. and Lewis, W.J. (Editors), 1981. Semiochemicals: their Role in Pest Control. Wiley, New York. Nowierski, R.M., 1979. The field ecology of the walnut aphid, Chromaphis juglandicola (Homoptera: Aphidae) and its introduced parasite Trioxys pallidus (Hymenoptera: Aphididae) a qualitative and quantitative assessment of population regulation. Ph.D. Dissertation, University of California, Berkeley.
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Parker, F.D., 1971. Management of pest populations by manipulating densities of both hosts and parasites through periodic releases. In: C.B. Huffaker (Editor), Biological Control. Plenum Press, New York, Chap. 16. Porter, B.A., 1947. Orchard insecticides. In: Yearbook of Agriculture, Washington, DC, pp. 659--662. Ratcliffe, F.N., 1965. Biological control. Aust. J. Sci., 28: 237--240. Ridgway, R.L. and Vinson, S.B. (Editors), 1977. Biological Control by Augmentation of Natural Enemies. Plenum Press, New York. Ripper, W.E., 1956. Effect of pesticides on balance of arthropod populations. Annu. Rev. Entomol., 1 : 403--438. Room, P.M., Harley, K.L.S., Forno, I.W. and Sands, D.P.A., 1981. Successful biological control of the floating weed salvini. Nature (London), 294 (5836): 78--80. Simmonds, F.J., Franz, J.M. and Sailer, R.I., 1976. History of biological control. In: C.B. Huffaker and P.S. Messenger (Editors), Theory and Practice of Biological Control. Academic Press, New York, Chap. 2. Smith, R.F. and Reynolds, H.T., 1977. Some economic implications of pesticide overuse in cotton. In: New Frontiers in Pest Management. Conf. Proc., Sacramento, CA, pp. 25--34. Snyder, W.C., Wallis, G.W. and Smith, S.N., 1976. Biological control of plant pathogens. In: C.B. Huffaker and P.S. Messenger (Editors), Theory and Practice of Biological Control. Academic Press, New York, pp. 521--539. Van den Bosch, R., Horn, R., Matteson, P., Frazer, B.D., Messenger, P.S. and David, C.S., 1979. Biological control of the walnut aphid in California: impact of the parasite, Trioxys pallidus. Hilgardia, 47: 1--13. Van Lenteren, J.C., Ramakers, P.M.J. and Woets, J., 1980. Integrated control of vegetable pests in greenhouses. In: Integrated Control of Insect Pests in the Netherlands, Pudoc, Wageningen, pp. 109--118. Volterra, V., 1927. Variazioni e fluttuazioni del numero d'individui in specie animali conviventi. Venezia, Premiate Officine Grafiche C. Ferrari (translated into English by F.M. Scudo and J.R. Ziegler, 1978. The Golden Age of Theoretical Ecology: 1923-1940. Springer-Verlag, Berlin, pp. 153--159). Wood, B.J., 1971. Development of integrated control programs for pests of tropical perennial crops in Malaysia. In: C.B. Huffaker (Editor), Biological Control. Plenum Press, New York, Chap. 19.