BIOLOGICAL CONTROL OF DECIDUOUS ORCHARD PESTS
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Deciduous orchard pests are increasingly targeted for classical biological control in an overall integrated pest control effort. Even partial reductions in the abundance of a pest in orchards can enhance the effectiveness of cultural methods and bait and pheromone trapping. Principal crops include almonds, apples, pears, peaches, cherries and walnuts (Minks & Gruys 1980, Croft 1982, Hoyt et al. 1983, Legner 1983a, 1983b; Legner & Silveira-Guido 1983, Legner & Goeden 1987, Legner et al. 1982a , 1982b,; Croft & AliNiazee 1996). For those pests in which almost no damage to the harvested fruit is acceptable, control by natural enemies is not sufficient as the sole source of control. Such pests include the codling moth, Cydia pomonella L., apple maggot, Rhagoletis pomonella (Walsh), cherry fruit flies, Rhagoletis cingulata Loew and Rhagoletis indifferens Curran, oriental fruit moth, Grapholitha molesta Busck, navel orangeworm, .Amyelois transitella (Walker) (see Research). In A. transitella a parasitoid, found in South America is being mass-produced and released annually in orchards. (See PHOTOS of Goniozus legneri Gordh). Although biological control can be effective against sporadic and some secondary pests such as mites, aphids and leafhoppers, the application of nonselective pesticides for control of a key pest may disrupt the balance in relationships of secondary pests with natural enemies so that pesticides often are implemented. At present there is reason to believe that some hasty applications of pesticides to such apparent imbalances may actually worsen the situations, and that no chemical treatments might have been the better strategy. Spiders are general predators that may well be preserved in orchards to combat phytophagous pests (Legner 1964 )
In a recent review, Croft and AliNiazee (1996) discuss biological control of deciduous orchard pests by dividing the effort into key, sporadic and secondary types. Key pests may attack the fruit directly and occur at damaging levels annually. Sporadic pests feed on either the fruit or other part of the tree or both, but are less common; and secondary pests are infrequently present unless disturbed by pesticides or other phenomena, and they usually feed on foliage and other non-fruit parts of the tree (Croft 1982). Biological control research has included various combinations of classical importation of natural enemies, augmentation of native and exotic species, conservation through cultural manipulation, utilization of natural enemy food sprays and selective pesticide deployment.
Natural enemies that have been directed against secondary pests have been most effective in deciduous orchards. Most research has involved endemic predators and using selective pesticides and improved cultural methods. Some success has been achieved with genetic improvement of pesticide resistant strains of predatory species (Hoy et al. 1983, Hoy 1985). The greatest effort has been in the conservation of natural enemies of plant feeding mites, aphids, leafminers and leafhoppers; however there has been little effort to introduce new exotic natural enemies to control these pests. This is partly because effective endemic species are thought to reside in most areas which are capable of providing significant control if they are properly managed. Similarly relatively little effort has been directed to augmentation because of the high costs involved.
Spider Mites.--Spider mites of the family Tetranychidae are important plant feeders which cause damage to deciduous fruit trees (van de Vrie et al. 1972, van de Vrie 1986). In non commercial orchards where no pesticides or poor horticultural practices are used, these mites are usually not problematic because of the activity of predator species. However, in commercial orchards which are fertilized, pruned and sprayed with pesticides, these mites often rise to high population levels exceeding 100 per leaf, resulting in fruit size and number reduction, and quality reduction. Trees may even be killed after several successive years of attack by dense populations.
Spider mites are controlled indirectly by implementing chemical control that is selective to certain key pests. Several different groups of predators are involved, such as Phytoseiidae and Stigmaeidae predators mites, coccinellid beetles in the genus Stethorus, hemipterans and neuropterans in the Chrysopidae and Hemerobiidae, and some predaceous thrips, spiders, etc. The most widely used natural enemies are phytoseiid mites and predatory Stethorus beetles. By monitoring populations of phytophagous mites, alternate prey and predators, it is possible to forecast predator/prey ratios early in the growth of pest populations (Croft 1982). When prey levels exceed certain levels, selective acaricides may be used to reduce phytophagous mites without influencing predators (Croft & McGroarty 1977, Mowery et al. 1977). The use of combinations of predators and selective acaricides can reduce acaricide usage 50-90%, and pesticide resistance development in spider mites can be slowed (Croft et al. 1987).
Alternative prey species of predatory mites may be enhanced. Examples include Aculus schlechtendali (Nalepa) as prey for Metaseiulus occidentalis (Nesbitt) in apples (Madsen 1968, Hoyt 1969), ground cover manipulations to enhance overwinter survivorship and early dispersal of Amblyseius fallacis (Garman) into trees (Croft & McGroarty 1977), alternate middle row application of pesticides to conserve Stethorus punctum (LeConte) (Hull & Beers 1985), and transferring foliage cuttings from trees infested with predators to areas lacking Typhlodromus pyri (Schenten) (Solomon & Easterbrook 1984).
Insecticide resistant predatory mites have been deployed in management with both resistance developed in the field and that resulting from genetic improvement through hybridization and artificial selection. In North America, and to some extent in Australia, New Zealand and Europe, resistant strains of Amblyseius fallacis, Typhlodromus pyri and Stethorus punctum have been used, which usually involved inter orchard movement of resistant strains. Successes with populations of Metaseiulus occidentalis having resistance to two or more pesticides have been accomplished (Croft & Strickler 1983, Hoy 1985, Croft & Roush 1988). When resistant natural enemies are selected in the laboratory, relatively low levels of recessive and polygenically determined resistance traits are maintained. However, this resistance is not stable under field conditions and might be lost by hybridization with susceptible native strains, thus making them difficult to manage (Croft 1983, Croft & Strickler 1983, Hoy 1985).
Aphids.--Several aphid species are major pests in deciduous orchards, including the apple aphid, Aphis pomi DeGeer, wooly apple aphid, Eriosoma lanigerum Hausmann), rosy apple aphid, Dysaphis plantaginea (Passerini) and green peach aphid, Myzus persicae (Sulzer). Myzus persicae is a vector of crop pathogens and thus the economic threshold is so low that biological control is usually not feasible; but possibilities exist with the other aphid species. The walnut aphid, Chromaphis juglandicola Kaltenbach and filbert aphid, Myzocallis coryli (Goetze) have been successfully attacked with classical biological control.
Classical biological control of aphids in deciduous orchards was emphasized for many years. For example, the woolly apple aphid parasitoid, Aphelinus mali (Hald.), originally found in eastern North America, was distributed to other parts of the this continent during 1921-1939 (DeBach 1964). This parasitoids has been introduced to over 50 different countries with successful establishment in about 42 (Clausen 1978). Results of parasitoid establishment were variable, but excellent control was reported in the Northwestern United States, Australia, Tasmania, British Columbia, New Zealand, Uruguay and Chile, while moderate control was reported from Europe and Asia. Attention has recently focused on Aphis pomi in Massachusetts with an examination of a cecidomyiid predator, Aphidoletes aphidimyza (Rondani). Adams & Prokopy (1977, 1980) documented resistance in this predatory fly to some organophosphate insecticides, and a number of selective pesticides were deployed. An aphid/predator ratio of 40:1 or lower was necessary to preclude selective pesticide treatment.
Warner & Croft (1982), Morse (1981) and Morse & Croft (1987) identified selective pesticides and examined predator/prey relationships of A. aphidimyza and A. pomi in Michigan apple orchards. Warner & Croft (1984) reported >12-fold resistance to azinphosmethyl in field populations and found phosalone, phosphamidon, carbophenothion, pirimicarb and several fungicides and acaricides to be relatively harmless to this dipteran predator. Morse & Croft (1987) found that a critical prey/predator ratio of 70-90:1 would provide adequate biological control of the aphid before an action threshold level of from 40-60 per terminal was reached. Predators such as Forficula auricularia L. and aphidiid braconid parasitoids have been investigated in Washington state (Carroll & Hoyt 1984a,b, 1985, 1986). Praon unicum Smith and Lysiphlebus testaceipes (Cresson) were significant biological control agents of the aphid early in the season in some orchards, even though they did not successfully develop through their entire life cycle while feeding on A. pomi. Alternate winter and summer aphid hosts of these parasitoids occurred on weeds and grasses in nearby peach orchards, with Myzus persicae being one of the major hosts on peaches. An insecticide tolerant earwig, Forficula auricularia was one important predator that prevented resurgences of A. pomi following treatments with selective pesticides. Augmentive releases of the earwig early in the growing season maintained aphids below 50/tree compared to 2-3,000/tree in orchard plots where earwigs were excluded or where releases were not made (Carroll & Hoyt 1986).
Effective natural enemies of the woolly apple aphid include a host specific aphelinid endoparasitoid Aphelinus mali and a complex of generalist predators in Washington State (Walker 1985). With the generalist predators excluded, A. mali was incapable of preventing aphids from soaring to unacceptable levels. The most important predator was Coccinella transversoguttata Fald in midsummer, the neuropteran Chrysoperla nigricornis (Burm.) and the mirid Dareaocoris brevis (Uhler) throughout the middle and later summer. Other generalist predators such as Adalia bipunctata (L.) were observed to be important natural enemies in Oregon (Croft & AliNiazee 1996).
French and Spanish strains of Trioxys pallidus Haliday have been used effectively in Oregon against the filbert aphid, Myzocallis coryli Goetze (Messing & AliNiazee 1988, Messing 1986), whereas the French and Iranian strain of T. pallidus successfully controlled walnut aphid, Chromaphis juglandicola (Kalt.) in California walnut growing areas, with different strains active in different areas, as previously discussed (Schlinger et al. 1960, van den Bosch et al. 1970).
Leafminers.--Leafminers in the genus Phyllonorycter sustain significant parasitism by parasitic Hymenoptera in the families Braconidae, Pteromalidae, Eulophidae and Ichneumonidae (Hagley et al. 1981. Wieres et al. 1982, van Driesche et al. 1985, Hagley 1985). There have been leafminer outbreaks reported from almost all parts of North America coincident with the development of resistance to pesticides and disruption of natural enemies (Pree et al. 1980, 1986; Wieres et al. 1982, Maier 1983, van Driesche et al. 1985, Trimble & Pree 1987). Impacts by the various leafminer natural enemies have been measured by Johnson et al. (1976), Hagley (1985), Ridgeway & Mahr (1985) and Barrett & Jorgensen (1986). Effects of pesticides on them were reported by Hagley et al. (1981), Weires et al. (1982) and van Driesche et al. (1985). Deployment of pesticides during periods when natural enemies were least vulnerable has been undertaken (Hagley et al. 1981, Weires et al. 1982, van Driesche et al. 1985). Temperature dependent phenological models of the emergence of pest and natural enemies, such as Sympiesis marylandensis Girault and Photesor ornigis (Weed), show rather narrow biological windows of invulnerability for the parasitoids (Drummond et al. 1985).
Leafhoppers.--The white apple leafhopper, Typhlocyba pomaria McAtee and several other less specific species, Empoasca fabae, Edwardsiana rosae and Erythroneura spp. attack deciduous orchards in North America (Sayedoleslami 1978, Elsner & Beers 1987). Resistance to organophosphate insecticides has gradually increased problems with leafhopper control (Croft & Hoyt 1983). Biological control has stressed egg and larval parasitoids. In Michigan, overwintering eggs of T. pomaria are attacked primarily by the mymirid Anagrus epos Girault, with parasitism ranging from 20-50% to 100% (Sayedoleslami & Croft 1980). Research has shown good synchrony between pest and natural enemy throughout orchard tree scaffolds. Parasitism by the nymphal-adult parasitoid Aphelopus typhlocyba was lower than egg parasitoids (Sayedoleslami 1978). Parasitoids seem to tolerate organophosphate insecticides such as azinphosmethyl which has been in use for a long time, so that field resistance is suspected (Croft 1982). In Washington, the white apple leafhopper eggs are heavily parasitized by Anagrus epos with a high degree of synchronization occurring between the host and parasitoid (Beers & Elsner 1988).
Croft and AliNiazee (1996) give some examples of classical biological control in deciduous orchard environments, such as spider mites, pear psylla, Psylla pyricola Foerster, codling moth, Cydia pomonella, apple maggot, Rhagoletis pomonella and other fruitflies, etc. However, detailed discussions of classical biological control of these and other orchard pests may be found under each pest's name separately in the section on case histories (CASEHIST.*).
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