BIOLOGICAL CONTROL IN GLASSHOUSES
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Tetranychus urticae Control with Phytoseiulus persimilis
Greenhouse Whitefly Control with Encarsia Formosa
Parrella & Hansen (1996) estimated that the world glasshouse area is 100-150,000 ha., divided equally between vegetable crops and ornamentals (van Lenteren 1987, van Lenteren & Woets 1988). Natural enemies may be more easily manipulated in the glasshouse environment because of the relatively uniform environment. Presently biological control is regularly implemented on ca. 3,000 ha. of glasshouses devoted primarily to vegetable production, although there is probably a much greater total world area involved, but data is lacking. Greathead (1976), Hussey (1985) and Lipa (1985) have reviewed the use of biological control in glasshouses.
Western Europe houses a large concentration of glasshouses, where there is a long tradition for practical application of biological control, and most information available originates in that area. The following treats in detail the use of biological control in vegetables and ornamental crops.
Biological control here is applied by the seasonal inoculative release method (van Lenteren 1983). Limited numbers of parasitoids or predators are liberated periodically in short-term crops of 6 to 9 months, in order to build up the population of beneficial organisms for control throughout the growing season. In some cases large number of natural enemies are released, in an inundative style, to obtain the immediate reduction of a pest population. The two systems that have been used extensively involve Phytoseiulus persimilis Athias-Henriot to control the two-spotted spider mite, Tetranychus urticae Koch and Encarsia formosa Gahan to control the greenhouse whitefly, Trialeurodes vaporariorum (Westwood). Recently efforts have also included leafminers, thrips and aphids. Biological control was traditionally applied on cucumber and tomato crops, which rank as the largest volume of vegetables grown in glasshouses, but has also expanded to include peppers, eggplants and melons. Biological control is the favored control method in Europe because chemical control interferes with harvesting schedules (Ramakers 1980a) and there is a higher risk of phytotoxicity during winter months (van Lenteren et al. 1980b). Young vegetables planted in winter are generally less vigorous and especially susceptible to pesticides. This conditions is aggravated by the application of carbon dioxide to improve yields (Hussey & Scopes 1977). In cucumber, yield increases of 20-25% are common in glasshouses using biological control compared to those with chemical control (Gould 1971).
Tetranychus urticae Control with Phytoseiulus persimilis
A principal pest of glasshouse crops is Tetranychus urticae (Hussey & Huffaker 1976). Spider mites are generally common on cucumber throughout the world, but their importance on tomatoes and sweet petter varies. These mites feed on the cell chloroplasts which causes a reduction in leaf photosynthetic activity. Damaged areas merge as the mite populations increase, causing the leaves to die.
Biological control of T. urticae is well suited to cucumber because the crop may tolerate damage up to 30% of leaf surface without a yield reduction (Hussey & Parr 1963). Since the discovery of P. persimilis by Dossee (1959), many researchers (Chant 1961, Bravenboer & Dosse 1962 have demonstrated the efficiency of this predator. Hussey et al. 1965. Legowski 1966, Gould 1968, Dixon 1973, French et al. 1976, Gould 1977). Acaricide in twospotted spider mites resistance further stimulated a reliance on this predator (Pruszynski 1979, Petitt & Osborne 1984, Osborne et al. 1985). Phytoseiulus persimilis possesses several attributes which make it an ideal predator under glasshouse conditions. AT temperatures of 15-35°C its developmental time is shorter than that of the prey, T. uriticae. At 20°C, P. persimilis and T. urticae increase at a rate of 4.6 and 2.7 times per week, respectively (Scopes 1985). Bravenboer & Dosse (1962) reported that the optimal temperature for developmental time, reproduction and feeding of P. persimilis was 25-30°C. Force (1967) obtained optimal control of T. urticae at a constant temperature of 25°C, where stable los density populations of both prey and predator were obtained, thus ensuring survival of the predator. However, at 30°C prey regulation ceased and at 20°C the prey was too quickly eradicated. In glasshouse environments there is considerably greater complexity than in the Force (1967) experiment), and both species tend to survive generally. Stenseth (1979) reported satisfactory control at temperatures of 15-27°C.
Several advantages of P. persimilis are (1) a high mobility, (2) voraciousness, (3) wholly dependent on T. urticae for food and (4) an avoidance of prey free environments (Chang 1961). Females do not feed on spider mite eggs, but migrate from a leaf when all active prey are eaten, but not before depositing their own eggs among those of T. urticae.
Dispersal within a glasshouse is great, every colony of spider mites in a glasshouse with cucumbers is associated with a predator only 18 days after introducing P. persimilis onto every 10th plant (Bravenboer 1971). The predator has been observed to spread to 10 tomato plants in 10 days (Hussey & Scopes 1977). Specific kairomones deposited on the leaves by the prey are attractive to the predator (Sabelis & van der Baan 1983). Within one spider mite colony P. persimilis detects its prey by random contact (Jackson & Ford 1973), but the predator remains in the colony until all prey are eliminated (Sabelis et al. 1984).
Phytoseiid predators have relatively low minimum food requirements for development and reproduction when compared with other natural enemies of spider mites. This accounts for their efficiency even at low prey densities (Hussey et al. 1965, McMurtry et al. 1970). Control is usually achieved rather rapidly, as shown by Chant (1961) who obtained control in 35 days, Hussey et al. (1964) in 22-33 days, by Force (1967) in 22 days at a predator:prey ratio of 8:20, and Stenseth (1979) within two weeks at an initial predator: prey ratio of 1:10.
The initial density of T. urticae for successful control of P. persimilis is very important (Hussey et al. 1965). An estimate of the pest density is obtained by the leaf damage index (Hussey & Par 1963) which relates the number of mites feeding per leaf to a visual ration. When predators are introduced at low densities, reduction of the pest population density is achieved before the economic injury level is attained. If plants are damaged to a mean density of 1.0 before predator introduction, reduction of the mite population occurs more quickly, but the economic injury level is exceeded.
Phytoseiulus persimilis is adversely affected by low relative humidities. Stenseth (1979) found that survival of the egg stage dropped from 99.7% at 80% RH to 7.5% at 40% RH and 27°C. Few predators were found to complete their larval development at 50% RH or lower over a range of temperatures (Pralavorio & Almaguel-Rojas 1980). Also at low RH adult longevity and fecundity of P. persimilis are encumbered. This predator tends to avoid excessive heat which normally occurs at the tops of cucumber plants in midsummer. They leave the apical foliage and hide beneath the lowest leaves, leaving T. urticae free to increase at the upper halves of the plants (Hussey & Scopes 1977). The problem can be averted by timing the original introduction of predators so as to achieve almost complete control of spider mites before warm temperatures occur (before June).
Introduction Methods For Phytoseiulus persimilis. Three different methods of introducing the predatory mites on vegetables are used. In the Patch method, predaceous mites are introduced at the site of the initial spider mite infestation that may be increased by diapausing female T. urticae. This is followed by introductions of P. persimilis on cucumber plants infested with T. urticae on which no predators have been discovered through sampling (Gould 1968, 1970, Stenseth 1980). This method is not too time consuming if inspections are conducted routinely during general plant care. In Denmark cucumber growers spend about eight hours a year per 1,000 m2 (Hansen et al. 1984a)
In the Pest-in-first method, cucumber plants are deliberately infested with T. urticae immediately after planting. After ca. 10 days P. persimilis is introduced on the same plants. This method gives the most predictable control (Hussey et al. 1965, Legowski 1966, Gould 1970, Dixon 1973, Hussey & Scopes 1977).
The Simultaneous Introduction method produces a uniform distribution of T. urticae and P. persimilis either before spider mite infestations are observed (Legowski 1966, Stenseth 1980) or at the first sign of leaf damage (French et al. 1976, Stenseth 1980). This method is preferred when large numbers of ex-diapausing females are expected in the glasshouse (Stenseth 1985).
Greenhouse Whitefly Control With Encarsia formosa
The greenhouse whitefly, T. vaporariorum has a wide host range, having been found on plants from 249 genera in 84 plant families (Russel 1977). Vet et al. (1980) provided a thorough review of whitefly pest problems and the use of E. formosa. This whitefly is considered a principal pest of vegetable crops in glasshouses, and is also very serious on tomatoes and cucumbers.
Trialeurodes vaporariorum feeds on the phloem of the plant, but the principal injury arises from the excretion of honeydew by all developmental stages. The honeydew gives rise to sooty molds, Cladosphaerospermum spp., which reduces photosynthesis and interferes with respiration (Hussey et al. 1958).
Encarsia formosa has been used commercially in Europe since 1927 with mixed success (Speyer 1927). The advent of synthetic organic pesticides in the 1940's temporarily discontinued its usage, however. Later with the development of resistance in another pest, T. urticae, growers were again dependent on predacious mites which also required an elimination of whitefly control of pesticides. More precise recommendations concerning the use of E. formosa then became available (Woets 1973, 1976, 1978, Parr et al. 1976). The efficiency of E. formosa is demonstrated by examining the rapid increase in the area on which this parasitoid was used during the 1980's.
Biological characteristics which make E. formosa a valuable biological control agent are is high searching capacity, parasitization efficiency, and host feeding behavior (Nell et al. 1976, van Lenteren et al. 1977, Hussey & Scopes 1977, Vet 1980, Eggenkamp-Rotteveel et al. 1982). The parasitoid may migrate over considerable distances (>10 m) from release sites, being attracted to volatile chemicals emitted by immature whiteflies and their honeydew. Infested plants are clearly preferred, as 90% of landings have been observed to be on infested leaves. In fact a single infested plant in a group of 28 can be singled out. There is discrimination between parasitized and healthy hosts, which decreases superparasitism. Host feeding occurs on unparasitized hosts only.
In the early 1970's when petroleum prices soared, it became necessary for growers to reduce average temperatures in glasshouses and to find tomato varieties that were suited to the lower temperatures (18/7° C D/N). The lower temperatures were at first considered harmful to parasitization efficiency of E. formosa whose intrinsic rate of natural increase was thought to be lower than the host at temperatures below 20°C. However, further research showed that temperatures between 12-25°C were still optimum for the parasitoid's performance (van Lenteren & Hulspas-Jordan 1983).
There is a robust functional response of E. formosa to its whitefly host on tomato (van Lenteren et al. 1977) on which successful biological control is easily achieved. In the case of cucumbers, however, parasitization is less efficient (Woets & van Lenteren 1976, van Lenteren et al. 1977). The longer surface hairs on cucumber retain honeydew, which reduces the searching efficiency of Encarsia, which must spend much time preening.
Light in the form of sunshine is an important stimulus to Encarsia, and RH of 50-70% is desirable (Milliron 1940, Parr et al. 1976). When the host gathers in dense patches, the accompanying honeydew interferes with parasitoid performance (Ekbom 1977).
Encarsia formosa is cultured in large quantities at small cost. It is able to survive handling and cold storage well. Parasitoids are introduced into glasshouses as pupae, which are highly protected by the larval skin of the host. It is important to introduce the parasitoid when whitefly densities are still low. An initial density of 10 adult hosts per 100 m2 is already too high (Ekbom 1977). A parasitization rate of >50% is necessary for control.
Introduction Methods For Encarsia formosa.--The Pest-in-first method involves deliberate infestation of the plants with whiteflies followed by several introductions of the parasitoid. This permits precise timing of parasitoid introductions to coincide with development of preferred 3rd instar hosts. Although reliable control may be obtained with this method (Gould et al. 1975, Parr et al. 1976), resistance of growers to introducing whiteflies into their crops has prevented its widespread adoption (Ekbom 1977, Stacey 1977). The Multiple Introduction or Dribble method involves successive, introductions of parasitoids starting right after planting. Four to 10 introductions of parasitoids are required to achieve success (Parr et al. 1976, Gould et al. 1975, Woets 1978, de Lara 1981). In cases where whiteflies are already apparent in glasshouses, other release rates are recommended (Ekbom 1977, Stenseth & Aase 1983, Hansen et al. 1984a). Sometimes plants with established populations of T. vaporariorum and E. formosas ( = Banker plants) are placed at intervals throughout the glasshouse (Stacey 1977).
Leafminer Control With Parasitoids
There are several species of leafminer pests found in glasshouses. The tomato leafminer, Liriomyza bryoniae Kaltenbach, is found on tomato, cucumber and melon crops in Western Europe. The pest status of this species increased after the mid 1970's when a change of growing substrate from soil to artificial media caused growers to abandon soil disinfection, which was largely responsible for controlling leafminer pupae. Therefore, leafminers began to overwinter in glasshouses. A relatively high infestation (15 mines per leaf) may be tolerated on tomato without yield loss (Wardlow 1985a), however young plants may be killed by the miners.
Three common parasitoids have given satisfactory control of leafminers in The Netherlands, England and Sweden. These are Dacnusa sibirica Telenga (Nedstam 1983), D. sibirica combined with Opius pallipes Wesmael (de Lara 1981, Woets & van den Linden 1982, Woets 1983), or D sibirica combined with Diglyphus isaea Walker (Wardlow 1984). The parasitoids overwinter in the glasshouse if soil disinfection is absent, such sources giving control in up to 60% of tomato glasshouses in the Netherlands. Diglyphus isaea often migrates into the glasshouses in July and August and can eradicate the Liriomyza bryoniae population through intensive host feeding activity (Woets & van den Linden 1985).
Both D. sibirica and O. pallipes, both endoparasitoids, have a shorter developmental time and lay more eggs than the host, and are able to recognize parasitized leafminer larvae (Hendrikse & Zucchi 1979, Hendrikse et al. 1980). Diglyphus isaea is an ectoparasitic species and is more difficult to handle and transport. In tomatoes, endoparasitoids are introduced as pupae within leafminer puparia when the first host larvae are observed. The numbers introduced must be sufficient to obtain a 90% parasitization of the second leafminer generation (Wardlow 1985a). Woets & van den Linden (1982) maintain that an introduction of O. pallipes corresponding to 3% of the total larvae in the first leafminer generation is necessary to achieve control.
Other leafminer species are problematic in North America. Of these Liriomyza trifolii (Burgess) and the vegetable leafminer, L. sativae Blanchard are most severe. Insecticide resistance is especially serious in the United States (Parrella 1987), and several researchers have investigated the potential of parasitoids to control L. trifolii (Lindquist & Casey 1983) and L. sativae (McClanahan 1980) on tomatoes.
Early in the 1980's L. trifolii invaded Europe and became established in glasshouses in The Netherlands and southern France. Promising results have been obtained in The Netherlands with the parasitoid Chrysocharis parksi Crawford introduced from California in combination with D. isaea (Woets & van den Linden 1985). A Mediterranean strain of D. isaea provides good control on tomato in southern France (Parrella & Robb 1985, Minkenberg & van Lenteren 1986, Parrella 1987).
Biological Control of Aphids
Many genera of aphids are present in glasshouses, some of which are polyphagous like the green peach aphid, Myzus persicae (Sulzer), the melon or cotton aphid, Aphis gossypii Glover, the potato aphid, Macrosiphus euphorbiae (Thomas) and the glasshouse or potato aphid, Aulacorthum solani Kaltenbach. All species exhibit rapid reproduction, with the species just named being capable of increases at rates of four to eight times per week at 20°C (Rabasse & Wyatt 1985). Damage results primarily by sucking plant juices, in particular from young developing plant tissue, leading to bud and leaf distortion. There is also severe damage caused by excretions of honeydew.
Despite numerous studies of aphidophagous insects, only a few species have been shown useful in glasshouses (Mackauer & Way 1976). The parasitoid Aphidius matricariae Hal. has given satisfactory control of M. persicae (van Lenteren et al. 1980b, Rabasse et al. 1983). This species is well adapted to glasshouse conditions and is often found to be the principal parasitoid when parasitoids have migrated naturally into a glasshouse. Ephedrus cerasicola Stary is another parasitoid that has shown promise (Hofsvang & Hagvar 1982).
In spite of such promising results, the commercial use of aphid parasitoids has not gained wide adoption (van Lenteren 1985). Perhaps this is because the outcome is unpredictable as the balance between aphids and their parasitoids is often upset by hyperparasitoids during early summer (van Lenteren et al. 1980b). Hussey & Bravenboer (1971) found that control can only be obtained when the rate of aphid population increase is suboptimal due to crowding or host plant resistance.
The cecidomyiid Aphidoletes aphidimyza (Rond.) is being used commercially to control aphids on vegetable crops in Finland, Denmark, Canada, the United States and the Soviet Union. Commercial mass production of this predator is on a large scale. Its success is due to its habit of feeding on all species of aphids, exhibiting a good functional response to increasing aphid density, its ease of mass production and transport, its ability to overwinter in glasshouses and a high adult mobility (Markkula & Tittanen 1985). The predator requires only seven M. persicae to complete development (Uygun 1971), and thus is able to survive during periods of prey scarcity. At high host densities it is able to kill up to 10 times this number of aphids.
Diapause is stimulated in A. aphidimyza by short daylengths (<15 hrs), which poses a problem in northern Europe (Hansen 1983). However, diapause is facultative and may be prevented by a L:D regime of 16:8 hrs. Gilkeson (1986) reports on selecting a strain of A. aphidimyza with a critical daylength of 9 hrs, allowing for its use as a predator during winter months.
Aphidoletes aphidimyza pupae are introduced into glasshouses when aphids are first observed at rates of one pupa per three aphids or 2-5 pupae per m2 (Markkula et al. 1979). Such introductions are repeated after 2-4 weeks in order to avoid synchronization of generations. The effect of A. aphidimyza on M. persicae on sweet pepper is often superior to chemical control. The "Banker plant" method is also used occasionally with this predator (Hansen 1983).
Thrips Control With Predatory Mites
Thrips have become increasingly more problematic in glasshouses in recent years, especially on cucumbers and sweet peppers. This increase in importance is also related to the adoption of artificial media and the subsequent lack of soil disinfection. Therefore, thrips are more often present in a glasshouse when a young crop is planted. Also there have been great reductions in blanket treatments of insecticides for other pests which used to aid thrips control. Drip irrigation systems with consequent drier atmospheric conditions in glasshouses and the raising of slow growing cucumber varieties may also explain the recent greater importance of thrips as pests.
Thrips tabaci Lindeman is the most common species on vegetables in Europe, whereas in North America the most common species on tomatoes and cucumbers is Frankliniella occidentalis. Thrips feed on plant sap after piercing tissues with the maxillary stylets and mandible, resulting in desiccated plant tissue. A relatively high density (<25 thrips per leaf) of thrips may be tolerated on cucumber (Hansen 1988). Here too chemical control of T. tabaci became impractical as Phytoseiulus persimilis became more important for spider mite control. Therefore there is presently widespread research being conducted to develop biological controls for thrips. This work is still at the experimental stage, with some progress already evident.
Ramakers (1980b) and Ramakers & van Lieburg (1982) reported promising results with native phytoseiid mites, Amblyseius barkeri (Hughes) (= A. makenziei Sch. & Pr.) and A. cucumeris (Oud.). Both predaceous mites show a pronounced association with thrips. In The Netherlands if mixed populations of both predaceous mites are introduced on sweet pepper, A. cucumeris consistently is the dominant species (Ramakers 1983). Amblyseius cucumeris is more difficult to culture, but seems to give better control on sweet pepper (Ramakers & van Lieburg 1982). In 1985 A. cucumeris was introduced on 68 ha. of sweet pepper by releasing predators early in the season and before the occurrence of thrips (Klerk & Ramakers 1986). Since A. cucumeris is a nonspecific predator, thrips need not be present at the time of predator introduction. In 83% of the nurseries control of thrips was completely successful. By 1986, the acreage on which A. cucumeris was applied was doubled to 140 ha. (Ravensberg & Altena 1987). Amblyseius barkeri is the more promising predator on cucumber, and in seven commercial glasshouses satisfactory control of T. tabaci was achieved using large numbers (Hansen 1988). Typically the thrips population increased during the first weeks after predator introduction, but then quickly crashed to low densities where it remained for the next few months. Predator densities were relatively constant throughout the sampling period and probably survived on other food sources.
Control success seems independent of release rates above a minimum of 3-400 predators per m2, and initial thrips densities seem rather important. In 13 commercial glasshouses with cucumber, introductions of large numbers of predators gave satisfactory control in only nine (Hansen 1988). Predators, which had been established successfully in all 13 glasshouses, were not significantly lower in density in those cases with unsatisfactory control, which may be explained by the increase rate of thrips on different varieties of cucumber. Generally, most of the beneficial species used for biological control of glasshouse pests are introduced in small numbers when the pest is first observed on the crop; the density usually in the order of 1-5 m2. With Amblyseius spp. for thrips control much large quantities are necessary, however. Klerk & Ramakers (1986) introduced an average of 24 A. cucumeris per m2 on sweet pepper, while on cucumber introductions of 300-600 A. barkeri per m2 provided satisfactory control of T. tabaci (Hansen 1988). This thrips disperses more quickly in the glasshouse than the predator, hence the difference in numbers of predators needed compared with other systems. Furthermore such nonspecific predators may be less efficient searchers at low prey densities, which is nevertheless compensated by low mass production costs.
Ornamentals are also attacked by many of the same pests which attack vegetable crops in glasshouses, but the number of pests on ornamentals is actually greater which is related to the diversity of crops in this category. Parrella & Hansen (1996) discuss why strategies developed for using natural enemies in vegetables cannot be directly transferred to ornamentals for several reasons. Most important is that ornamentals have a much lower economic threshold for insect damage, thereby placing serious constraints on natural enemies. Pesticides are, therefore, applied on a regular scheduled basis to a variety of crops year-round. Such practices are not conducive to biological control. The higher value of ornamental crops together with the potentially large losses associated with even moderate insect damage justifies the indiscriminant use of insecticides to many growers (Newman & Parrella 1986). Additionally, biological control alternatives are more costly than growers are willing to pay as they must be applied more often than chemicals. Hussey & Scopes (1985) stated that there have been a number of attempts to use biological control on short term crops but these have not been supported by basic research and most introductions failed. Although growers may be willing to try biological control, without specific guidelines for their situation, success is doubtful.
However, there are several factors which actually favor the adoption of biological control methods in ornamentals, particularly in the production of chrysanthemums and roses. Chrysanthemums are one of the major floricultural crops grown throughout the world, with ca. 2,350 ha. in Japan, The Netherlands, Germany, Colombia and the United States (Anonymous 1982). They are grown either for cut flowers, garden bedding plants or potted flowering plants. Biological control is usually only possible for cut flowers because of the longer duration of growth in glasshouses (Scopes 1970).
Leafminers, aphids and thrips are the major insect problems, with minor pests including mealybugs, several Lepidoptera, plant bugs and spider mites. Relatively few comprehensive studies have been made for biological controls of these pests integrated into overall IPM strategies (Scopes & Biggerstaff 1973, Price et al. 1980, Wardlow 1985b, 1986, Parrella & Jones 1987).
Aphid species of major importance that damage chrysanthemums are M. persicae, A. gossypii, the leaf curling plum aphid, Brachycaudus helichrysi (Kaltenbach), and the chrysanthemum aphid, Macrosiphoniella sanborni (Gillette). Because of the broad-spectrum insecticides applied to chrysanthemums in the United States, the last named species is rarely a problem there. Natural enemies investigated for biological control have included Coccinellidae, Chrysopidae, Cecidomyiidae, Syrphidae and fungi (Gurney & Hussey 1970, Scopes 1969, Hall & Burgess 1979, Markkula & Tittanen 1985, Chambers 1986).
Rabasse & Wyatt (1985) determined that the distribution of aphids varies vertically on chrysanthemum plants as well as between varieties for each of the aphid species. Therefore, to establish a uniform density of predators over an entire chrysanthemum crop requires regular predator releases, which are usually prohibitive in cost. Some success was obtained with the predatory midge, Aphidoletes aphidimyza Rond. because of its high searching ability and relatively low cost of culture. A disadvantage with this predator has been its low fecundity, which may not be as important as at first believed (Gilkeson 1987). The syrphid fly, Metasyrphius corollae (F.) has also been promising (Chambers 1986), even though a pollen source is required to initiate gametogenesis and both adults and larvae respond poorly to low aphid densities. Both of these predators are more likely to succeed in biological control when they are combined with other control options such as the use of fungi and parasitoids.
Many species of parasitoids are commonly associated with aphids that develop on chrysanthemums, but natural migration into the glasshouse is too slow for them to reduce damage significantly (Wyatt 1970). In California it has been observed that Diaretiella rapae (M'Intosh) and Lysiphlebus spp. migrate into chrysanthemum glasshouses in response to M. persicae populations but satisfactory control was never observed. Inundating with parasitoids has not been evaluated although Scopes (1970) tried to establish Aphidius matricariae early in the life of a chrysanthemum crop by distributing parasitized aphids on aphid-infested cuttings in the boxes of cuttings prior to planting. Wyatt (1965) found that biological control was more feasible on those cultivars which are not especially good hosts for aphids.
The fungus Cephalosporium lecanii (VertalecR) is widely used to control aphids on chrysanthemums in Europe (Hall 1985); however it is not commercially available in the United States as of 1991 (Markle 1985). This fungus is not equally effective against all species of aphids, with decreasing order of sensitivity found in M. persicae, B. helichrysi, A. gossypii and M. sanborni. It is thought that the registration of Vertalec in the United States is of paramount importance for the success of biological control on chrysanthemums. Registration for the selective aphidicide, primiarb, has been lost and the only materials available to growers that control aphids are broad spectrum biocides. In Europe this material is primarily used during April to September because pulling shade cloth during this period increases RH and favors the development of epizootics. In coastal areas where most of the chrysanthemum industry is located in California, RH may be high enough all year for the fungus to be effective (Parrella & Hansen 1996). Zoophthera erinacea is another potentially important aphid specific fungus, which has been found on chrysanthemum in Colombia, but no culture procedure has been developed (Hall 1985).
Lepidoptera commonly attack chrysanthemums (Jarrett 1985) with the beet armyworm, Spodoptera exigua Hübner and the tomato moth, Lacanobia oleracea being most severe. Research has focused on biological insecticides (e.g., Bacillus thuringiensis Berliner var. Kurstaki) with special emphasis on formulations and strains that are particularly effective against Spodoptra. There is also a promising granulosis virus for S. exigua (Vlak et al. 1982).
Lygus bugs will migrate into glasshouses in Europe and the United States (Wardlow 1985b, Jones et al. 1986) where they feed on developing terminals and young buds, thereby virtually destroying the crop. There are no tested biological control options for these insects.
Spider mites, especially Tetranychus urticae Koch, can cause problems on chrysanthemums, with some cultivars being more sensitive than others. Application of the predator Phytoseiulus persimilis Anthias-Henriot at the rate of one per 50 plant cuttings gave excellent control (Scopes & Biggerstaff 1973). Wardlow (1986) recommended releasing this predator every week at the rate of 10 predators for every 200 plants. (also see Osborne et al. 1985).
Citrus mealybug, Planococcus citri (Risso) has been a problem on chrysanthemums (Whitcomb 1940). The predaceous coccinellid Cryptolaemus montrouzieri Mulsant was successfully used with releases at the rate of one adult predator for every two plants. Experiments with the coccinellid and the parasitoid Leptomastix dactylopii Howard have shown that this combination can successfully control P. citri on crotons, Pilea, Clivia and Cattleya (Copeland et al. 1985).
Leafminers attacking chrysanthemum include two important species, Liriomyza trifolii (Burgess) and Chromatomyia syngenesiae (Hardy), the latter having invaded North America from Europe (Spencer 1973). Although C. syngenesiae is resistant to insecticides (Hussey 1969), L. trifolii is still tolerant to a wide range of pesticides (Parrella & Keil 1985, Lindquist et al. 1984). Liriomyza trifolii is currently spreading throughout Europe (Powell 1982). In England the braconid Dacnusa spp. are applied at the rate of 3 adults per 1,000 chrysanthemum plants one week after planting, followed by introduction of the eulophid, Diglyphus isaea at 3 adults per 1,000 plants six weeks after planting (Wardlow 1985b, 1986). The use of Diglyphus spp. has also been recommended for L. trifolii, with regular weekly releases necessary for control (Jones et al. 1986, Gaviria et al. 1982). Cultural controls are regularly integrated with parasitoids for leafminer control (Price et al. 1980, Wardlow 1985b, 1986, Parrella & Jones 1987).
Integrated pest management including biological controls is prevalent on roses grown in glasshouses. Parrella & Hansen (1996) estimated that roses are grown on about 2,900 ha. in Holland, Germany, United States, Italy, France, Japan and Israel. The culture is essentially perennial as budded stock plants are used which produce roses for many years. The same plant can be productive for >10 yrs. Thus although a relatively stable environment is created, roses are susceptible to many diseases which require almost regular applications of fungicides (Hasek 1980), and little is known of the compatibility of such fungicides with natural enemies. The principal arthropod problems are twospotted spider mites, flower thrips, aphids and leafrollers.
In France IPM involves releases of P. persimilis for control of T. urticae (Pralavorio et al. 1985). But because environmental conditions in glasshouses vary considerably from one locality to another, there is no general guideline possible for IPM (van Lenteren et al. 1980a). Parrella & Hansen (1996) disagreed with Smith & Webb (1977) that biological control is less likely to be successful in North America than in Europe in glasshouses, pointing out that specific programs for roses and other crops must be developed for different growing areas.
Phytoseiulus persimilis was found to give consistent results on roses in the United States when an economic threshold of 10 mites per leaflet was established (Boys & Burbutis 1972). In California good results were obtained with Metaseiulus occidentalis (Nesbitt) for T. urticae control on glasshouse roses. This predators was integrated into the pest control program because of an insecticide resistance capability, and it persisted in glasshouses for more than two years (Field & Hoy 1984).
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