Key words: Harmonia axyridis, Multicolored Asian Lady Beetle, Biological control

Biological control, or the use of living organisms to control other organisms, is becoming a more important tool in IPM programs than ever before. Every year pesticides commonly used to control particular pest insect situations are either becoming less effective due to resistance, or unavailable because of proven health hazards to non-target organisms.

The multicolor Asian lady beetle, Harmonia axyridis, is an introduced biological control native to Western Asia. It was first introduced into North America in 1916 in California, and again in many states in the Eastern United States between 1978 and 1982. It was not recorded as collected until 1988 in Louisiana. Since that time it has proven to be a voracious feeder on soft-bodied homopteran pests, as well as being highly competitive with native species of Coccinellidae. Additionally, it has acquired a bad reputation stemming from its autumn habit of aggregating on, and invasion of houses and buildings in search of overwintering sites.

In the Asian lady beetle’s native habitat, its migration takes it to light colored rocky cliffs and outcroppings. In North America, migrations more often orient to light colored buildings where adult beetles can cover sunny south facing walls by the thousands. The lady beetles then search for cracks and crevices in the structure where they enter to overwinter. Beetles that successfully enter buildings eventually aggregate in secluded dark places. Their ability to reflex bleed, leaving stains on walls, curtains, etc., distinctive odor, and habit of becoming active on warm days has led to their additional designation as an insect pest.

Research investigating ways of dealing with this beneficial insects aggregation behavior are looking at various aspects of the insect’s behavior and cues triggering the behavior. Trials involving the use of plant derived natural products such as menthol and camphor, used as repellants, have show promise, although the persistence of formulations available at the present is not adequate. Additionally one research group is attempting to determine the cues that trigger the aggregation behavior, in an attempt to possibly create a product that would cue the beetles to go to a specific trap instead of a house or building.

When introducing new species into ecosystems there are prices to pay that are often unanticipated. Although this insect has proven to be an excellent biocontrol agent when viewing shear numbers of homopteran pests consumed, it has also proven to be an annoying pest in its own right, to the species that brought it here.

This paper will look at the impact, and attempts to manipulate the behavior of an introduced biological control agent Harmonia axyridis Pallas (Coleoptera: Coccinellidae) the multicolored Asian lady beetle, as it is more commonly known. Biological control is defined as the action of natural enemies toward a pest population, maintaining it at levels that are tolerable. Since the first major success in classical biological control of insect pests, when cottony-cushion scale Icerya purchasi Maskell (Homoptera: Margarodidae) was brought under complete control in California by introducing two natural enemies, vedelia beetle, Rodolia cardinalis Mulsant (Coleoptera: Coccinellidae) and the parasitic fly, Cryptochaetum iceryae Williston (Diptera: Cryptochaetidae), introduced biological control agents have shown throughout the world, and over the years, that biological control can be achieved through introduction of natural enemies onto a population of insect pests.

But release of these non-native insects does not go without risks that can temper the reward sought. Successful biological control always has ecological consequences, as does any pest control method, or even doing nothing. Of particular concern for biological control is the affect on non-target hosts. The goal is to introduce species that are relatively host-specific, so as to not impact other species of organism in the ecosystem, possibly throwing another part of the system out of kilter. Additionally, biological control agents are free to go where they please, so their impact is not restricted to a client’s property as is typical for a pesticide.

Since part of the goal when releasing biological control agents is to have them become extremely abundant, so they can have an impact on the population of the targeted pest insect, they often become a nuisance in there own right. This applies in many cases, such as the massive population of the beneficial weevil Neochetina eichhorniae Hustache (Coleoptera: Curculionidae) that in the autumn leaves the collapsing populations of water hyacinth in the southern United States to congregate around mercury vapor lights . This also has occurred in the case of the recently established multicolored Asian lady beetle that reportedly has become a nuisance to homeowners during autumn, when large numbers alight on the exterior of buildings, then move into dark, protected cracks and corners to overwinter. Subsequently, they re-emerge, throughout the winter without breaking diapause, from wall voids, baseboards, etc., and may fly around rooms for hours at a time . They have also been reported as a honeybee pest where they invade hives in the winter, using the hive as an overwintering site. Their presence may clog up the covers and reduce upward ventilation of the overwintering bee cluster .

Adult Harmonia axyridis beetles are oval and convex in shape, 5 to 8 mm in length. Their head is straw yellow, antennae and mouthparts are yellow-brown, sometimes tinged with black. The pronotum is straw yellow with four black spots that are reminiscent of the shape of a W or an M (depending on how the insect is viewed). These polymorphic beetles have elytra that range from pale yellow-orange to bright red-orange, often with up to 20 black spots, although the spots can be reduced or absent. The larvae are distinctive when compared with native or previously established coccinellid larvae. Their elongate, flattened bodies are covered with tubercle and spines, which makes them bristly in appearance. Mature larvae, which are overall black to dark bluish-gray, exhibit an unbroken longitudinal orange strip down each side of their body . The pupae are predominantly orange, with minimal black markings (personal observation). Eggs are bright yellow, laid in clusters of about 20 on the undersides of leaves.

The multicolored Asian lady beetle distribution up to its establishment in North America was Asia and Australia, where its prey consists of mostly homopteran insects such as psyllids and scale. It was widely distributed in Asia, where it is recorded from Formosa, China, Korea, Japan, Manchuria, southern Siberia, and the Ryukyu and Bonin Islands. There it is viewed as an arboreal species that mostly occurs in orchard and forest habitats.

The first reports of this beetle being introduced into North America occurred in California in 1916, 1964, and 1965, by the U.S. Department of Agriculture. These releases were unsuccessful in establishing Harmonia axyridis into North America, as well as subsequent releases in Nova Scotia, Connecticut, District of Columbia, Delaware, Georgia, Louisiana, Maine, Maryland, Mississippi, Ohio, Pennsylvania, and Washington from 1978 to 1982. Specimens were also released in Connecticut in 1985. The multicolored Asian lady beetle was first reported to be established in North America in Louisiana and Mississippi in 1988. The only releases of the beetles in Louisiana or Mississippi consisted of one release of 32 specimens in Shreveport, Louisiana in 1979, and eight releases of a total of 3781 specimens in Mississippi in 1980. Ironically, it is believed that the lady beetle established populations resulted from an accidental introduction of the species during freighter activity in New Orleans . The first reports of establishment on the west coast occurred ten years after the intentional release of the beetles in King County, Washington, in 1991.

Currently H. axyridis has spread into the eastern half of the country, and ranges from Florida to Quebec and west to Texas and Missouri. It is also reported from Washington, Oregon, Colorado (personal observation) and British Columbia, Canada.

One of the chief concerns when dealing with release of biological control agents is what other organisms will the control agent have an effect on besides the pest that it has been brought to control. In the case of Harmonia axyridis this has been a major, and warranted concern. H. axyridis are not host specific, many soft-bodied insect can be part of their diet, and they will feed on other beneficial insect species, such as other cocinellid larvae.

In apple orchards of eastern West Virginia twenty- five species of Coccinellidae were found from 1983 to 1996. From 1989 through 1994, the exotic coccinellid, Coccinella septempunctata (first collected in 1983), dominated in numbers between all of the species found. H. axyridis displaced C. septempunctata in 1997, and is providing better biological control of Aphis spiraecola on apple in eastern West Virginia . Although H. axyridis has been a beneficial addition in the apple agroecosystem, it, along with the other exotic species, C. septempunctata, constituted over 70% of the individuals collected, quickly edging out native species and greatly affecting the coccinelline fauna of West Virginia apple orchards.

Intraguild predation has been documented in laboratory situations as well. H. axyridis larvae fed on a diet of Coleomegilla maculata (Coleoptera:Coccinellidae) eggs can complete development, and predation between H. axyridis and C. maculata larvae usually results in H. axyridis eating C. maculata . Previous to the study it had been noted that H. axyridis adult and larvae combined were the second most frequently observed predator species feeding on C. maculata eggs on sweet corn, additionally, an observation was made of a late-instar H. axyridis eating a late-instar C. maculata on sweet corn in the field (T. E. Cottrell, pers. obs.).

Trials and observations in recent years such as these have led to an increasing concern about the environmental impact of biological control introductions. In a Michigan study a monitoring system was established within a variety of cultivated and natural habitats in order to characterize the first 5 years of establishment of H. axyridis. Population trends for 11 coccinellid species were followed, and annual population increase, habitat utilization patterns, and within-season population fluctuations for H axyridis were analyzed. Coccinellid species showed a decline in abundance after the arrival of H. axyridis, however the decline cannot be attributed to H. axyridis without further assessment. H. axyridis showed great adaptability in habitat. Although thought of as an arboreal species, it was also found present in agricultural habitats such as forage crops, corn, soybean and wheat. Population increases of H. axyridis since 1994 were steady and substantial. In 1994, they accounted for 2.8% of the coccinellids captured that year. In 1995 and 1996 they accounted for 5.6 and 13.6% respectively, of the coccinellids captured. In 1997 H. axyridis became the dominant species of the coccinellids measured in the study. In only four years from its detection in southern Michigan it became a dominant coccinellid .

Coccinellid species have frequently been shown to exhibit aggregation behaviors. Hippodamia convergens (Guer.), the convergent ladybeetle, has been commonly observed on the shores of lakes in the Upper Midwest during summer and autumn. The beetles remain on the shore for only a short time, usually dispersing within 2-3 weeks. The beetles in these shore aggregations may be so numerous that 5000-10,000 living individuals may be collected in one hour . J. R. Douglass, an entomologist for the U.S. Bureau of Entomology, wrote one of the first published reports of lady beetle aggregation behavior in 1930. He observed for several years, from 1925 through 1929, aggregations of ‘thousands’ of Hippodamia convergens (Guer.), on Mosca Peak in the Manzano Mountain Range, 30 miles southeast of Albuquerque, New Mexico . The reasons for these aggregations range from accidental collection when migrating beetles are blown into water and washed ashore, as is the speculated case with the aggregations formed on the shores of lakes, to the mountain top aggregations that appear to be winter insect hibernation behavior, or diapause, a part of the life cycle of many coccinellid species.

In the autumn the multicolored Asian lady beetle adults prepare to go into diapause. In their native environment in Kyoto, Japan, they were frequently found aggregating within the cracks and crevices of rock outcropping, but aggregations were also found inside a wooden hut. Beetles appeared to orient toward light-colored objects within these sites . In North America, since their introduction and establishment, it has been reported that they become a nuisance to homeowners because of this aggregation behavior and subsequent winter hibernation.

Their typical behavior includes alighting en mass on the exterior light colored buildings, often buildings that are isolated from other building and tall structures. They then move into dark, protected fissures and recesses to overwinter. They remain in the dark, protected areas throughout the winter, periodically becoming active, and emerging to wander around the inside of the structure, often times flying around the building for hours. Complaints from human inhabitants of the invaded buildings include staining of walls and furniture from reflex bleeding and fecal material, odor, and general annoyance of the beetles flying around light and encroaching on cooking, sleeping, bathing and recreational activities .

Until H. axyridis was introduced into the United States there was little incentive to explore the mechanisms responsible for coccinellid aggregation behavior. The annoying habit of aggregation in such close proximity to humans has changed that attitude. The pursuit for a working knowledge of the cues that trigger or regulate aggregation in this coccinellid has begun so as to develop management strategies that would exploit cues and taxis responses that the insect is found to employ in its aggregation behavior. The combination of issues involved in addressing a biological control agent as a potential pest have created a unique challenge for researchers and pest control agents. There is an urgent need to discover how to safely thwart the entry of these otherwise desirable lady beetles into buildings without killing them. Research has focused mostly on looking at determining aggregation cues used by the lady beetles, and repellant products that may influence chemotactic responses of the beetle.

There is no evidence that secondary cues responsible for influencing decision making on the part of the beetle in orienting to aggregation sites in autumn involve volatile aggregation pheromones. Chemical cues may mediate the final stages of aggregation behavior in H. axyridis, and may be based on contact chemoreception with conspecifics, or the feces and residues that persist in aggregation sites from previous years. Visual cues appear to play a large role in aggregation site selection, as potential beetle shelters situated in heavily wooded sites often attract no beetles . The accumulated evidence suggests that first, individuals respond independently to environmental cues, leading to aggregation in an optimum location. Second, individuals respond to chemical and /or thigmotactic stimuli provided by other individuals, leading to aggregations in specific microhabitats within that location.

Early stage management strategies based on the evidence gathered in research on aggregation behavior cues indicate that because houses serve as visual super stimuli, any method of initially deflecting aggregating swarms from a home would involve installing surfaces that are taller, more reflective and possibly larger than the home in question. After beetles arrive at a site, it may be possible to direct their movement via secondary cues such as chemoreception of conspecifics or feces. Keeping the live insects in a chosen site, however, may be problematic; because of winter flight activity redistribution would likely occur.

The potential for modifying the behavior of the multicolored Asian lady beetle via negative chemotactic properties of particular plant-derived products has been evaluated. Monoterpenoids camphor and menthol were both effective in repelling adult beetles in bioassays and field studies. Field experiments with the use of sprayed formulations of camphor or menthol into crevices on the exterior of a building through which beetles were entering showed that camphor was superior to menthol . Within 48 hours after the crevice was sprayed beetles were no longer repelled by menthol or camphor, indicating that repellant treatments would need to be closely spaced during aggregation activity, or persistence of these chemicals must be extended.

Any successful biological control attempt has an ecological impact. The beneficial impact of multicolored Asian lady beetle has been shown through its superior control of insect pest Aphis spiraecola in apple orchards in eastern West Virginia , three pest species on pecan trees in Las Cruces, New Mexico , as well as numerous other pest situations. The negative impact has continued to grow, as the population of H. axyridis has continued to grow and spread, affecting more people every year in a very direct manner with its aggregation behavior. To these people the beneficial qualities go unnoticed, and to them it is not considered a success story in the long line of introduced biological control agents.

Opposition to biological control species introductions may become more of an issue if situations such as this one continue to occur without adequate solution development. The research presented in this paper reveals that management of these nuisance beetles may be achieved by a push-pull strategy. The use of repellent chemicals such as camphor could provide the ‘push’ to keep beetles away from structures where they are a nuisance, and then ‘pulling’ them into baited shelters with chemical attractants such as conspecific, fecal, and aggregation site persistent residue volatiles.

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