Development of behavioral-based pest management alternatives has been necessitated by the loss of traditional pesticides, insect pest resistance, pest resurgences, secondary pest outbreaks often due to the detrimental effect of pesticides on non-target organisms, the rising cost of pesticide development, and public concerns about environmental and health issues. The use of behavioral chemicals, which include general categories of feeding stimulants and semiochemicals, have broad potential applicability.

This review article evaluates palatability studies of a variety of naturally occurring substances that have been tested for feeding stimulant/semiochemical properties on a number of key economic pests. Many studies, though not all of those reviewed, found that sucrose was one of the more effective sugar feeding stimulants.

Several researchers tested commercial nutrient-based phagostimulants, and reported widely varying consumption results. Semiochemical-based toxic baits take behavioral-based pest management tools to a higher level. Research also exists on semiochemicals that include entomopathogens, including viruses, and Bacillus thuringiensis.

Many researchers state that semiochemical-based baits are a potential tool in greatly reducing the amount of pesticides applied and in increasing the efficiency of insecticidal baits on a variety of major economic crop production systems, even though some of the research has not shown positive results.

Introduction

Over the past half-century, the heavy reliance on broad-spectrum insecticides, and their associated challenges, has been well-documented (Ridgeway et al., 1991). That insect pests continue to impact agronomic and horticultural crops necessitates continued emerging, innovative pest control technologies. A broad category of potential insect control technologies involves the use of behavioral chemicals. Use of behavioral chemicals (including the general categories of feeding stimulants and semiochemicals) may in fact allow the application of reduced dosages of insecticides assuaging some of the environmental and health concerns associated with traditional insect control tactics.

Early work focused on "poisoned sweets" and bait pails to control various insect pests (Ditman & Cory, 1933). Sugars are one of the best documented groups of substances as to their feeding stimulant potential (Adler, 1989; Allsopp, 1992; Bartlet et al., 1994; Ditman & Cory, 1933; Ladd, 1986 & 1988; Lopez et al., 1994a & 1996). Several other substances that may have feeding stimulant properties are amino acids, ascorbic acid, and glucosinolates (Allsopp, 1992; Bartlet et al., 1994; Lopez et al., 1994a), cucurbitacins (Metcalf et al., 1987), and garbanzo beans (Potter & Watson, 1983a). As interest mounted in nutrient based feeding stimulants, a variety of commercial phagostimulants have been developed. Several researchers (Farrar & Ridgeway 1994; Lopez & Lingren, 1994b) have trialed these products to determine which elicited the strongest feeding responses.

In addition to the commercialization of some feeding stimulants, semiochemical-based toxic baits have become the focus of much research (Brust & Foster, 1995; Chandler, 1993 & 1998; Lance & Sutter, 1990 & 1992; Weissling & Meinke, 1991). The addition of feeding stimulants to entomopathogens (Bartelt et al., 1990; Hough-Goldstein et al., 1991; Potter & Watson 1983b; and Salama et al., 1985) has in some cases increased the effectiveness of the control.

Feeding stimulants – sugars

Sugars are phagostimulants for most insects (Bartlet et al., 1994). Determining palatability, that is, which sugars provoke the best responses, was an important question that early researchers such as Ditman & Cory (1933) sought to answer. Ditman’s study intended to narrow the field of sugars that would need to be tested in further bait work. Newly emerged corn earworm, Helicoverpa zea (Boddie) moths were tested on 10 different sugars in solution (chemically pure sugars and distilled water). Of the sugars tested, sucrose, invert sugar, and fructose were the most attractive. Of the remaining sugars, glucose received the best response, maltose and xylose were attractive at strong concentrations, arabinose and galactose were only slightly attractive, while mannose and lactose drew no reaction. Results were compounded by certain insects becoming sugar sensitive, or sugar non-sensitive; some moths never ceased to respond to water, whereas others never responded even to strong molar concentrations of sugars.

In contrast, Alder (1989) reported that the kind of sugar (fructose, glucose, or sucrose) did not affect feeding rate of corn earworm moths, though rates did change (decrease) with time, within a feeding session, and from day to day. Alder also found no significant differences in fecundity and longevity between the three sugars tested. Lopez’s (1994a) work used corn earworm proboscis extension response to screen 12 sugars as feeding stimulants. Sugars evaluated were fructose, fucose, galactose, glucose, maltose, melezitose, raffinose, rhamnose, ribose, sorbose, sucrose, and turanose. Lopez reported results that were similar to Ditman’s, in that moths had higher and more uniform responses to sucrose and fructose but not to glucose. Response to the other sugars was variable with low proboscis extension response, suggesting that these sugars do not show as much promise as feeding stimulants for adult corn earworms.

An additional Lopez (1996) study evaluated the potential of dry sucrose as a feeding substrate for corn earworm. Using dry sugars, or other materials, as opposed to sugars in the liquid phase would certainly simplify the development and use of attracticidal baits, as they would be easier to incorporate into bait formulations, and also would be easier to apply and would persist longer in field applications. The study produced indirect evidence that the liquid necessary for the digestion of the dry sucrose was secreted from the salivary glands and not as reguritant from the crop. Moths allowed to feed on a liquid sucrose solution prior to feeding on dry sucrose ingested 3 times as much total sucrose as those fed only dry sucrose. These results suggest that proboscis secretion may limit the amount of dry sucrose that can be ingested by corn earworms.

Sugar responses have also been tested on several major insect pests belonging to the order Coleoptera. Ladd (1986 & 1988) studied feeding responses of Japanese beetle, Popillia japonica (Newman) adults and larvae respectively, to a wide variety of sugars. Of the fifteen sugars tested sucrose, maltose, glucose and fructose were strong Japanese beetle adult phagostimulants, whereas xylose, arabinose, and raffinose demonstrated weaker, but significant, feeding stimulant potential. In addition to the same four sugars that elicited strong phagostimulant responses in adults, trehalose was an attractant for Japanese beetle larva (third instar). Evidently metamorphosis did not have any effect on the chemoreceptors that respond to the four sugars. Interestingly, trehalose is found in larvae hemolymph. Ladd (1988) speculated that perhaps the aggressive behavior of larvae biting one another when in confined areas might be related to the presence of trehalose. Of four sugars (fructose, glucose, sucrose and rhamnose) tested for feeding response from cabbage stem flea beetles, Psylliodes chrysocephala (L.), sucrose was the most effective, though all except for rhamnose stimulated feeding (Bartlet et al., 1994). In addition, Allsopp (1992) tested feeding response of 14 sugars to several sugar cane infesting scarabaeids (third instar), and reported that sucrose and fructose produced the strongest responses.

Feeding stimulants – other substances

There are many other substances that have been tested for phagostimulant properties on a variety of insect pests. Several have elicited postive feeding responses. Allsopp (1992), for example tested amino acids tyrosine, cysteine, glutamic acid, and histidine monohydrochloride, and reported significant feeding stimulation in several sugar cane infesting scarabaeids. In other research, Bartlet et al. (1994) tested a variety of glucosinolates, all of which increased feeding of cabbage stem flea beetle on agar (glucobrassicin was the most effective, and sinigrin the least). Dried and ground bitter squash roots and fruits, containing cucurbitacins, induced several corn rootworms, Diabroticite beetles, to feed on poisoned baits, increasing the kill proportionately (Metcalf et al., 1987). Fresh and dried garbanzo bean extracts were positive phagostimulants for the tobacco budworm, Heliothis virescens (Potter & Watson 1983a).

On the other hand, ascorbic acid was shown to elicit no significant feeding response for several sugar-cane infesting scarabaeids (Allsopp, 1992).

Commercial phagostimulants

The commercialization of appropriate pest management technologies may potentially allow faster implementation of these practices. Several commercial nutrient-based phagostimulant comparative studies have tested these products on a variety of Lepidopterous insect pests. Commercial phagostimulant brand names include Coax, Entice, Gusto Konsume, Mo-Bait, and Pheast. Lopez & Lingren (1994b) tested adult corn earworm proboscis extension response to these commercial feeding stimulants, in comparison with deionized water and 5% (wt:vol) sucrose solution. There was a significant age effect of response to the treatments, but there was no sex effect. Feeding rate increased over time. Adults of both sexes ingested significantly greater amounts of 5% sucrose solution than any of the commercial nutrient-based treatments. No significant differences were determined between the amount of water and commercial treatments. "It is possible that the feeding stimulant value of the phagostimulants could be enhanced by increasing the sucrose content" (Lopez & Lingren, 1994b).

In a separate study by Farrar & Ridgeway (1994), all of the above mentioned commercial feeding stimulants were tested, except for Konsume. Trial Lepidopterous insect pests included corn earworn, Helicoverpa zea (Boddie), gypsy moth, Lymantria dispar (L.), fall armyworm, Spodoptera frugiperda (J. E. Smith), beet armyworm, S. exigua (Hubner), European corn borer, Ostrinia nubilalis (Hubner), and diamondback moth, Plutella xylostella (L.). Large differences in consumption were seen between the different phagostimulants when tested on cellulose-agar media. Those differences were reduced when plant tissue was used as the substrate. Results indicated that commercial formulations with higher percentages of protein evidenced the strongest responses over formulations that contained mostly sugar. Mo-Bait was the least effective, as it contains the lowest amount of protein, and may have limited pest management use for any of the insect pests tested. Results from the other products varied. Pheast consistently was the most effective, and does have a slightly higher protein content. All of the commercial formulations, except for Mo-Bait improved the acceptability of the plant material. The efficacy of commercial phagostimulants has been questioned, but their potential in combination with entomopathogens is thought to be worthy of further investigation (Farrar & Ridgeway, 1994), and will be discussed later in this review article.

Semiochemical-based toxic baits

Semiochemical-based toxic baits are a potential tool for greatly reducing the amount of insecticide used to protect crops. These toxic baits can combine in dry bran, or starch-based carriers a feeding stimulant, and either an insecticide or insect growth regulator. A further refinement of semiochemical-based toxic baits is to add to the bait either a floral or non-pheromonal volatile attractant.

Research on corn rootworm is extensive, because several corn rootworm species, Diabrotica sp., are the most destructive pests of the northern corn belt. Corn rootworm insecticidal baits can be made more effective by the addition of semiochemicals. Lance & Sutter (1990) performed lab and field-cage tests using baits containing carbaryl as a toxicant, cucurbitacin as a feeding stimulant, and a nonpheromonal attractant. These components were encapsulated into starch granules. In field-cages treated with starch granules, numbers of beetles were reduced by 69-94%. The cucurbitacin feeding stimulant component appeared to be the key ingredient, whereas the nonpheromonal attractant did not have a measurable effect on the efficacy of the bait. General bait efficacy declined after 2-3 weeks in the field.

Carrying this research one step further, Lance & Sutter (1992) formulated a bait containing carbaryl, cucurbitacin, and several nonpheromonal volatile attractants in a dry, bran-based carrier. The field results were disappointing, as the bait activity was short-lived, with beetle population increasing again after 4-9 days and returned to pretreatment levels within 1-2 weeks. The reduced efficacy of the field applications was thought to be due to particle distribution, with a good proportion falling to the ground where beetles were less likely to encounter the bait. Bait that sticks to corn foliage would improve pest management efficacy.

Further corn rootworm, semiochemical-based toxic bait research was carried out by Weissling & Meinke (1991). They investigated whether a starch matrix could deliver granular, controlled-release semiochemical-insecticides (this starch matrix concept has already been successfully applied to herbicides and Bacillus thuringiensis). Beetle mortality was low, and may have been due to loss of carbaryl during the formulation process.

The most serious crop pest of cucurbits is the striped cucumber beetle, Acalymma vittatum (F.). The beetle not only defoliates the crop, but also transmits the causal agent of bacterial wilt disease. Brust & Foster (1995) compared a standard, weekly carbaryl spray schedule with a semiochemical-based toxic bait application. The bait contained carbaryl, cucurbitacin, and several floral attractants. The bait did reduce beetle numbers (and used only one tenth the amount of insecticide), but not as quickly as the standard carbaryl spray. However, the bait’s longevity was 7 days, whereas the beetle population continued to increase in the standard carbaryl plots. Additionally, more flowers were pollinated, and early fruit production was increased in the bait plots.

Another semiochemical bait combination was tested on fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith) by Chandler (1993). Bait was composed of a commercial phagostimulant (Coax, Konsume, or Nu-Lure) and one of several insect growth regulators (IGR’s). Growers have not readily accepted IGR’s as there is a longer period between treatment and death than with chemical insecticides. Phagostimulants may have the potential to shorten this critical interval between treatment and death. The addition of Konsume improved and enhanced IGR-effected mortality, and should be considered a viable alternative by crop managers.

Whereas, the previous studies investigated varying bait formulations, a recent study by Chandler (1998) compared several aerial semiochemical-insecticide bait application methods to control corn earworm. The formulated bait contains a cucurbitacin, carbaryl, and a carrier. Results indicated that broadcast treatments are more effective (control rate of 90-95%) at reducing adult numbers than alternating swaths.

Obviously, that this type of research has inherent complexities should be of no great surprise. Factors that can compound research results include: insect-host plant relationships, relationships among semiochemical components, bait particle size, efficacy, and persistence in the field, optimal bait formulation, choice of insecticide, rate of application, and application method. Despite the complexities, behavioral chemicals do offer an array of alternative pest management options.

Semiochemical-based baits and entomopathogens

A yet further refinement in semiochemical-based bait research is to include entomopathogens, either bacterial or virus. Many researchers chose starch encapsulation as a means of protecting the entomopathogen from environmental degradation, and enabling better persistence in the field. Starch palatability is an important issue that Bartelt et al. (1990) investigated. Starch granules, without feeding stimulant additives, were seldom fed upon, hence the addition of phagostimulants is necessary. In greenhouse tests, the commercial phagostimulant Coax elicited the greatest feeding response in European corn borer larvae, Ostrinia nubilalis (Hubner). As with semiochemical-insecticide baits, semiochemical-entomopathogen baits can reduce the amount of entomopathogen needed to effectively control the target pest. The Bartelt et al. (1990) investigation reported that the amount of B. thuringiensis applied could be reduced by 75%.

Further research both supports and challenges bacterial entomopahtogen effectiveness. For example, Coax was found to increase mortality of the cotton leafworm, Spodoptera littoralis when used as an adjuvant to increase the efficacy of B. thuringiensis (Salama et al., 1985). In contrast, Hough-Goldstein et al. (1991) only reported marginal increase in feeding by the Colorado potato beetle, Lepinotarsa decemlineata (Say), by the addition of feeding stimulants to a bait containing Bacillus thuringiensis var. san diego (M-One). Mortality was not increased significantly beyond results obtained when M-One was used without stimulants.

Virus entomopathogens have also been combined with feeding stimulants to increase their pest control effectiveness. Potter & Watson (1983b) reported the increased larval mortality of the tobacco budworm, Heliothis virescens (F.) when the virus was applied in conjunction with the commercial phagostimulant Coax. Increased larval exposure to plant material increases the probability of the larvae ingesting a lethal dose of virus.

Conclusion

Development of innovative pest control technologies that are economically feasible and socially acceptable is dependent upon gaining sufficient knowledge to be able to formulate reasonable solutions. Generally, new pest management techniques must be cheaper than existing tools to be adopted. However, growing awareness of environmental issues complicates economic imperatives. Pest management tools must be seen to be safe for both the environment and the public. Therefore, pest management tools that use behavioral chemicals could satisfy the above economic and social criteria. Feeding stimulants and semiochemical-based baits often both reduce insecticide use and increase the efficacy of the insecticide or entomopathogen used. In feeding stimulant and semiochemical research, complexities abound, but research does suggest that no one study has provided solid evidence that a single compound acts individually; hence it may be more likely that a positive response is due to a complex profile of compounds (Hedin et al., 1974). Realistic use of feeding stimulants and semiochemical-based baits to protect agronomic and horticultural crops will evolve with each generation of research inquiries.

References