A variety of insect and mite pests are found on potato. Those with the greatest opportunities for biological control in the context of integrated pest management are the Colorado potato beetle, Leptinotarsa decemlineata, and the green peach aphid, Myzus persicae. We will focus our presentation on these two species, but also provide examples of some other insect pests when appropriate. Some background on the general principles of biological control in integrated pest management will be useful to understand the benefits and cost of biological control in potato production.
Introduction to principles of biological
Biological control is the science of purposefully enhancing the activities of beneficial species to reduce the damaging activities of pest species. It represents the foundation or starting point for sound integrated pest management (IPM) (Stern et al., 1959). Biological control takes three forms in practice: classical, conservation, and augmentative.
In classical biological control natural enemies are sought in the native range of a pest insect, imported and established in an area where they do not naturally occur. Typically this is a geographic area where the pest has colonized and is substantially free of natural enemies from their native range. The biological control provided by the introduced natural enemies results in long-term reduction of the pest populations in selected habitats. Typically, classical control has been most successful in perennial agroecosystems such as tree crops, vineyards, ornamental plantings, and forests. Although dramatic successes have resulted from biological control introductions, the outcome is far from predictable. Only about 30% of introductions have resulted in establishments and successful pest suppression has occurred much less frequently (Hall and Ehler 1979). Key to the success of most biological control projects is the discovery and importation of natural enemies that produce high levels of parasitism or predation in the native range of the pest (Hawkins and Cornell 1994). Other factors, such as adaptation of the natural enemies to the climate of the new range and adequate searching and host utilization abilities to allow discovery and control of the pest when it is still of low abundance, are also thought to be critical.
Conservation biological control is the true underpinning of IPM (Stern et al.1959). Its goal is to foster natural enemy abundance by reducing harmful influences and enhancing positive ones. This may entail replacing a broad-spectrum insecticide for a species specific tactic or a narrow-spectrum insecticide, changing the timing of insecticide use to avoid periods when natural enemies are most exposed, providing alternate habitats for natural enemy to feed, reproduce or over-winter, by providing nectar - either through ground cover plants or by selecting a plant variety that has nectaries as food for adult natural enemies.
Augmentative biological control consists of two types of efforts: inoculative and inundative control. When seasonal agricultural practices interfere directly with natural enemies or with the availability of host or prey populations, natural enemy populations may be reduced to such a degree that they may be unable to catch up to rapidly increasing pests and prevent pest damage of the commodity before harvest. Inoculative control can be used to address these seasonally repeating problems that is typical of annual cropping systems such as potatoes. Natural enemies can be introduced earlier in the season than they would normally occur, giving them time to reproduce and suppress pests earlier in the cropping cycle. Inoculative biological control is the foundation for pest control in many glass house production systems (Van Lenteren and Woets, 1988) and has been attempted for potatoes as described below. Inundative approaches differ from classical and inoculative strategies, in that the activity of the released natural enemies -- and not their offspring -- are the active agents of control. Typically, large-scale releases of natural enemies are made and repeated many times during the cropping cycle.
So where does biological control using insects and pathogens fit into potato management? A review of the more notable beneficial insect species and pathogens that attack Colorado potato beetle and green peach aphid is provided below to provide some insight on this subject.
Predators and parasites of the Colorado
A number of arthropod species attack eggs, larvae, or adults of the Colorado potato beetle, and it is inferred that natural enemies provide some level of biological control of the beetle (Hough-Goldstein et al., 1993; Hilbeck and Kennedy, 1996, Hough-Goldstein 1998). In this section, we review predators and parasites of this species, summarize the current consensus view of their importance, and provide some idea where future research may be indicated to improve their efficacy.
- predatory bugs
Two species of Pentatomidae are known as effective predators of Colorado potato beetle: the spined soldier bug, Podisus maculiventris; and, the twospotted stinkbug, Perillus bioculatus. A third species, Opolomus dichrous, has also been studied, but does not appear to be well-adapted to cooler potato growing regions (Ferro 1994).
Of the three species, P. bioculatus has received the most study. This predator feeds on all stages of the beetle, although feeding on adults appears to be uncommon and probably is restricted mostly to the adult predator. A single bug may consume over 300 eggs of the beetle during its development (Tamaki and Butt, 1978). Second instar nymphs of the predator consume approximately 5 newly hatched beetles per day, or almost 30 larvae per nymph over the duration of that instar.
Naturally occurring densities of this predator appear to be too low to control the beetle below economically damaging levels, thus considerable attention has been paid to using inundative releases. The predator has been reared in large numbers in insectaries, and studies have been conducted using insectary-reared bugs to determine impact on Colorado potato beetle under field-conditions. Releases of P. bioculatus at the rate of 1 per plant caused reductions in beetle densities of about 30%, while releases of 3 per plant reduced beetle numbers by 60% (Biever and Chauvin, 1992). Combining releases of P. bioculatus with use of a microbial pathogen may provide better control of the beetle than either organism by itself (Poprawski et al., 1997; Cloutier and Jean, 1998). Attempts to establish Perillus as a classical biological control agent in Europe have proven unsuccessful (Jermy, 1980).
It is unlikely that these predators can be reared economically enough to be used in inundative releases under commercial conditions (Ferro, 1994). Moreover, despite considerable research, it remains unclear as to what timing of release or rate of release is most effective in controlling the beetle. More basic research on the biology of this species outside of potato fields is warranted so we may realize opportunities to modify habitats near potato fields to enhance the abundance of Perillus. Finally, more research is needed regarding compatibility of these predators with other control products, both biological and chemical.
Ladybugs (Coccinellidae) can be common in potato fields particularly if aphids are present. Some species may feed extensively on eggs of Colorado potato beetle, most notably, Coleomegilla maculata, a common predator in eastern U.S. potato fields. This species often builds to high densities late in the season in corn. It moves into overwintering sites from corn and the following spring can move into neighboring potato fields (Ferro 1994). Laboratory trials indicate that a single adult C. maculata consumes more than 10 eggs of Colorado potato beetle per day, but consumption rate drops when aphids are present in the crop. Studies by Hazzard et al. (1991) indicated that predation of eggs in potato plots in Massachusetts varied between 40 and 58%, most of which was attributed to the activity of C. maculata. No significant tests of inundative releases of C. maculata for suppression of Colorado potato beetle have been published.
Ground beetles (Carabidae) are common predators in unsprayed fields of potatoes, but their impact on Colorado potato beetle for the most part is not known. This is partly so because in most of the potato fields that have been examined, a complex of carabid species are found and their feeding activity is either cryptic or nocturnal. Laboratory studies have shown that a number of different species of ground beetles feed on Colorado potato beetle, in both choice and no-choice tests (Ferro, 1994). One species, Lebia grandis, has been shown to actively feed on eggs of Colorado potato beetle, consuming over 45 eggs per day per predator. Larvae of this predator are ectoparasites of the prepupal stage of Colorado potato beetle (Groden, cited in Ferro 1994). Sorokin (1981), Boiteau (1983) and others provide additional information on the predatory activity of carabids on Colorado potato beetle.
Carabids are much too slow growing and difficult to rear to be considered for augmentative forms of biological control. However, recent conservation experiments --use of straw mulch in potato plots--has shown that the number of middle instars of first generation Colorado potato beetle (mid May to mid-June) can be significantly reduced due to predation attributed to carabids (Brust 1994). In the same study, predation of eggs and young larvae of the second generation of the beetle (late June through July) was increased with straw mulch when Coleomagilla, lacewings, and Perillus were the most abundant predators found on potato plants. Together, the activity of these predators reduced potato damage and enhanced yield by 30% or more. Straw mulch provides a safe haven for predators, increases biodiversity in the mulch layer, and is likely to provide beneficial effects on insect pathogens in the soil, microbes that support plant growth, and enhance soil moisture.
Myiopharus doryphorae is a tachinid parasitoid of larval Colorado potato beetle. The adult fly injects maggots into the body of larval beetles. Parasitism by the fly typically does not build until later in the season and second generation larvae of the beetle usually suffer much higher parasitism rates than first generation (Tamaki et al., 1983). Thus effectiveness of this parasite in controlling the beetle under commercial situations may be low. However, parasitism rates approaching 70% have been noted in both potato and nearby wild host plants (Solanum saccharoides) in the spring in Colorado (Horton and Capinera, 1987). No significant effort at modifying habitats surrounding potato to harbor alternative hosts of the beetle, and thus M. doryphorae, have been attempted.
Edovum puttleri is a Eulophid parasite of the eggs of Colorado potato beetle . It was first found in Columbia attacking a close relative of Colorado potato beetle and was subsequently found attacking Colorado potato beetle in Mexico (Logan et al., 1987). Attempts to establish this species as a classical control agent of the beetle failed because the wasp has no diapause that would allow it to pass the winters in our northern production areas. Augmentative releases of Edovum were abundantly tested in the last decade. In one study, early season releases of E. puttleri caused 50% egg parasitism of the beetle. Its efficacy is underestimated by parasitism rate alone, because killing of eggs by probing, without parasitism, may often exceed parasitism rates (Lashomb et al., 1987). Finally, Edovum is known to depend on aphid honey dew as energy source, but aphids are typically not very abundant in potato until July. Additional studies of Edovum, particularly in the western production areas are warranted.
Species of Neuroptera (lacewings), Hymenoptera (vespid wasps), Nabidae (damsel bugs), Araneae (spiders), Lygaeidae (big-eyed bugs), and Reduviidae (assassin bugs) have been reported to feed on eggs, larvae, or adults of Colorado potato beetle. In general, their impact on the beetle under commercial conditions is unknown but recent studies using predator exclusion cages show that egg survival is increased 3 fold if predators are excluded (Hilbeck et al. 1997). Important in that study was the demonstration that predation activity was independent of beetle density. Thus the use of other nondisruptive tactics that lower beetle populations are fully compatible with the activity of the general guild of predators. Studies to foster predators as a larger complex of miscellaneous species, such as through the use of straw mulch cited above, are warranted in western production areas.
Green peach aphid
Van Emden et al. (1969) summarized the literature on green peach aphid and reported that 150 different species of insects are known to feed on this pest, of which a third (51 of 150) are members of the Coccinellidae. The other dominant taxa include the hoverflies (Syrphidae; 49 of 150) and lacewings (Neuroptera; 25 of 150). The list of van Emden is highly dated, and certainly more records are now available.
Numerous studies in different crops have shown that arthropod natural enemies suppress green peach aphid, and it is not possible to review those studies in their entirety here. Laboratory studies have compared feeding rates of different predator species, to provide information about what taxa might be most effective in the field. For example, Tamaki and Olsen (1977) showed a 10-fold difference in daily consumption rates of a certain ladybug beetle (53 aphids consumed per day) compared to a certain predatory bug (minute pirate bug; 5 aphids consumed per day).
Tamaki (1981) considers that ladybug beetles may be of particular importance in suppressing green peach aphid in potatoes, but emphasizes that the whole predator complex (comprising big-eyed bugs, damsel bugs, hoverflies, lacewings, and minute pirate bugs) must be considered in any biological control program for potato. Timing of aphid infestation, timing of predator infestation, and densities of immigrating pest and predators are critical in determining whether natural enemies successfully suppress the pest in potatoes.
A broad diversity of parasitic Hymenoptera, most notably in the families Braconidae (Aphidiinae) and Aphelinidae parasitize aphids. Pike et al. (2000) report several species from the green peach aphid in the Northwest of the USA from the aphidiine genera Aphidius, Diaeretiella, Ephedrus, Lysiphlebus, and Praon. Two Old World parasitic wasps, Aphidius colemani and A. matricariae, that attack green peach aphid are now established in Washington's potato production areas. A. matricariae appears to have a high preference for green peach aphid, and is rapidly becoming common in green peach aphid field collections. Most of the main insecticides used on potatoes in the past have adversely impacted beneficial insects, including parasitic Hymenoptera. In the future, as more selective materials such as Success® and Fulfill® become primary products of use, parasite and predator survival and presence in potatoes will increase. An additional Old World parasite, Praon gallicum, discovered attacking green peach aphid in 2000 in western Washington, is now in culture at WSU-Prosser, and will be mass-reared in early 2001 and subsequently released against green peach aphid in eastern Washington. These newly released species are enhancing and will continue to enhance the existing pool of beneficials, and will impact green peach aphid populations not only on potatoes, but also on herbaceous weeds. These parasites will not eliminate the aphid, but they are expected to play a more important role in the future as softer chemicals come into wider use.
Aphid parasitoids are readily mass produced but their potential for augmentative releases early in the season before aphids become numerous has not been adequately studied. The cultivation of wild plants that harbor early season aphids that would serve as alternative hosts or "bridge species " to enhance early season parasitoid abundance has also not been studied systematically.
The major problem in relying on biological control to manage green peach aphid in potatoes is that the major damage caused by the aphid is due to its virus-vectoring capabilities. There is little evidence that aphids become abundant enough to cause yield reduction or direct damage in cultivated potato. Because of this, only extremely low densities of the aphid are tolerated in commercial potato fields, particularly in July when aphids fly into potato from other hosts. Thus, even if natural enemies were highly effective at suppressing the aphid at low densities, numbers may still be high enough to cause economic damage due to vectoring of virus pathogens. Serious study of predators and parasitoids for biological control of green peach aphid in commercial fields will not occur until virus problems are solved. Current work to breed or engineer virus resistant potato varieties is very promising.
Pathogens of potato pest insects
Numerous pathogenic organisms have been discovered with biological control potential against insect pests, including those that attack potato (Burges, 1981; Tanada and Kaya, 1993; Poprawski and Wraight, 2000). We will focus on those with the greatest potential for successful microbial control. Procedures for the application and evaluation on microbial control agents in potato are presented by Poprawski and Wraight (2000). Several insect pathogens have a number of advantages over conventional chemical pesticides (Tanada and Kaya, 1993; Kaya and Lacey, 2000).
Although the advantages of microbial pesticides are many, there are also disadvantages. These include:
Bacteria for control of Colorado potato beetle
The discovery and development of Bacillus thuringiensis var. tenebrionis in Germany (Langenbruch et al., 1985) with activity against certain beetles in the family Chrysomelidae has resulted in selective and effective control of the Colorado potato beetle. Other strains with activity against the beetle have since been discovered and developed by Baum et al. (1996) and others. The larvicidal activity of the bacterium is due to the parasporal crystal that is produced by the bacterium at the time of sporulation. Protein toxins in the parasporal crystal , collectively known as delta endotoxins, must be ingested in order to be active. After being eaten, the crystal is solubilized in the alkaline environment of the midgut and enzymatically activated. The portion of the toxin molecule that is responsible for larvicidal activity, binds to specific sites on the membrane of the midgut cells and disrupts osmotic balance in the midgut cells. The cells swell and ultimately rupture allowing gut contents to enter the body cavity. The insects die shortly afterward. Sublethal dosages result in decreased foliage consumption and reduced survival, delayed development and emergence (Nault et al., 2000) and reduced longevity and fecundity in adults that were exposed as larvae (Costa et al., 2000).
A number of factors influence the larvicidal activity of Bt, such as the age of targeted larvae, temperature, spray rate and coverage of the plants, timing and number of applications and inactivation by sunlight. Younger larvae are the most susceptible (Zehnder and Gelernter, 1989). Although adults are not susceptible, they may be repelled by Bt-treated plants (Ghidiu et al., 1996).
Beetle active formulations of Bt have been produced by several companies and marketed for control of Colorado potato beetle. The results of field trials in North America have been reported by Ferro and Gelernter (1989), Zehnder and Gelernter (1989), Ferro and Lyon (1991), Zehnder et al. (1992), Ghidiu and Zehnder (1993) and Lacey et al. (1999) and other researchers. Control comparable to that of certain chemical pesticides is possible using label rates especially when application is made when the majority of the first generation is in the first and second instars. Research conducted in Washington State on the Raven product containing an engineered strain of Bt revealed that excellent protection of potato foliage was obtained with label rates (1.2 to 7.0 liter/ha) applied four times at weekly interval resulting in good tuber yield (33-40 tonnes/ha) (Lacey et al. 1999).
Distinct advantages of Bt formulations over that of conventional chemical pesticides are its safety for applicators and field workers and lack of activity on nontarget organisms, including natural enemies. In the irrigated desert of Washington State, the insect biodiversity in Bt treated plots was unaffected. However in aldicarb (Temik) treated plots, certain hemipterous predators were nearly eliminated (Lacey et at., 1999).
control of Colorado potato beetle and green peach aphid
Fungal pathogens are important natural enemies of a wide variety of insect and mite pests in virtually every agroecosystem (Goettel et al., 2000). The potato pests that have been best studied for the potential of fungi as natural enemies and microbial control agents are the green peach aphid and Colorado potato beetle. Fungi have also been reported from wireworms, leafhoppers, and other insect pests of potato, but their potential as microbial control agents has received limited attention.
Fungus for control of the Colorado potato
Other species of fungi have been isolated from Colorado potato beetle, but Beauveria bassiana has thus far been shown to be the most effective in controlling the beetle. This fungus belongs in the order Hyphomycetes in which reproduction is simple and does not involve a sexual stage. Beauveria bassiana and other members of this group can be grown on artificial media and are easily harvested (Feng et al., 1994 ;Goettel and Inglis, 1997). The fungus can be stored for fairly long periods especially when formulated and kept cool. Formulation of spores also enables application of the fungus using conventional spray equipment.
Beauveria bassiana has been produced by several companies and marketed for control of Colorado potato beetle and several other insects (Feng et al. 1994). The results of field trials have been highly variable ranging from unacceptable levels of control (Fargues et al., 1980; Hajek et al. 1987) to effective control (Hajek et al. 1987; Poprawski et al. 1997). Factors that effect its larvicidal activity include: temperature, humidity, age and stage of the insects, timing and number of applications, dosage, agricultural practices, and deactivation by sunlight (Fargues, 1972; Fargues et al., 1996). The fungus invades the insect's body, usually through the cuticle. After invading the host, the fungus grows throughout the body and under proper conditions, will sporulate on the surface of the host cadaver. This may take place on the host plant or in the soil prior to or during the pupation stage. Another benefit of using B. bassiana is overwintering adults may also become infected in the soil. The production of secondary inoculum on the host insect may contribute to increased mortality both on the host plant and in the soil. In addition to killing larvae, the fungus has been reported to slow the feeding rate of beetles that have received a sublethal infection (Fargues et al., 1994).
Fungal pathogens of aphids
Fungi are the only insect pathogens currently used for control of aphids (Hall, 1981; Latgé and Papierok, 1988). Because aphids obtain their food with piercing and sucking mouthparts, pathogens that must be ingested, such as bacteria and virus, are not be effective. Several fungi in the order Entomophthorales are important pathogens of aphids, including economically important species on potato (Latgé and Papierok, 1988). These fungi have more complex life cycles than the Hyphomycetes and, under conditions of high humidity, are often responsible for epizootics and crashes in aphid populations. Although they can cause dramatic crashes in aphid populations, reliance upon natural epizootics in most agroecosystems is risky. Very low densities of the green peach aphid may be detrimental to potatoes due to the transmission of leaf roll virus and other plant pathogens. In the absence of disease transmission, epizootics can provide benefit by severely reducing numbers of aphids below economic thresholds (Steinkraus, 2000). It is important to note that some agricultural practices may interfere with fungi and other natural enemies of potato pests insects. Langnaoui and Radcliffe (1998) reported that certain fungicides used to control plant disease in potatoes could interfere with infection of the green peach aphid.
A fungal species with good to excellent activity against the green peach aphid in humid environments is Verticillium lecanii (Hall, 1981; Burges, 2000). However, the use of V. lecanii and other Hyphomycetes for control of aphids in potato has not yet been investigated in detail. In the irrigated desert of the Pacific Northwest humidity may not be sufficiently high to enable rapid germination and infection. Furthermore, the lack of quick kill is inconsistent with managing this virus vector as discussed above.
The majority viral pathogens used in microbial control are baculoviruses applied against Lepidoptera. Certain species of Lepidoptera have been reported as defoliators of potato, but their importance is variable and eclipsed by the Colorado potato beetle. The most serious lepidopteran pest of potato in the Americas is the potato tuber moth, Phthorimaea operculella (Gelechiidae). Larvae can mine foliage and attack tubers in the soil or storage where they tunnel through the flesh of the potato. In addition to causing direct damage they facilitate entry and damage by secondary pests and diseases. Only one virus is currently used against a potato pest insects in the Americas. Pilot programs that employ the granulovirus of the potato tuber moth have had remarkable success in South America and are markedly safer and more sustainable than chemical alternatives. Most tuber moth virus production is done on a cottage scale.
Integration of Biological Control into
Integrated Pest Management
Sustainable agriculture in the 21st century will rely increasingly on alternative interventions to chemical pesticides for pest management that are environmentally friendly and reduce the amount of human contact with pesticides. The IPM strategy, in which natural enemies (parasites, predators and pathogens) of pest arthropods and other alternative measures play significant roles in crop protection (Hoy & Herzog 1985), can contribute to a more sustainable approach of for management of pests in potato production (Boiteau et al., 1995; Cloutier et al., 1995). However, a truly integrated approach in all agricultural practices will be required to obtain the maximum effect from a given intervention or practice without interfering with the effectiveness of other practices (Edwards 1990).