Robert L. Koch

Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America

The multicolored Asian lady beetle, Harmonia axyridis (Pallas), native to Asia, has recently been detected in South America after successfully invading North America and Europe. This coccinellid is a voracious predator; therefore, it is popular and effective in biological control. Unfortunately, H. axyridis also has associated adverse impacts (i.e., as a household pest, pest of fruit production, and threat to non-target organisms). To predict the potential geographic extent of impacts of H. axyridis in South America we review the history of its invasion in the Western Hemisphere and address various factors critical to the future invasion (i.e., arrival, establishment, and spread) of new areas of South America. The likelihood of continued introductions (i.e., arrival) of H. axyridis to South America seems high, due to its popularity as a biological control agent and through accidental introductions. Establishment also seems likely in broad regions of South America. Climate matching with the native range suggested that much of southern South America may be suitable for establishment. In contrast, habitat matching with the native range suggested that northern South America may be more suitable. In addition, prey availability should not limit establishment of this predator. Once established, H. axyridis seems likely to spread by flight and human-assisted means. Overall, the invasion of H. axyridis over broad areas in South America seems likely.

The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae)

Abstract The potential for a classical biological control agent, Harmonia axyridis (Pallas), to have non-target effects on populations of the monarch butterfly, Danaus plexippus (L.), was examined using no-choice predation studies under laboratory and caged field conditions. Three separate laboratory functional response experiments were conducted with adult and larval H. axyridis preying on immature D. plexippus . Nonlinear functional responses for third instar H. axyridis preying on D. plexippus eggs and first instars reached plateaus at about 25 and 15 prey consumed per day, respectively. A linear response resulted for adult H. axyridis preying on D. plexippus eggs. Potted Asclepias syriaca L. placed into large field-cages were infested with first instar D. plexippus and third instar H. axyridis . Survival of first instar D. plexippus was significantly lower in cages with H. axyridis larvae than in cages without H. axyridis larvae. The present experiments identify H. axyridis as a potential stressor to populations of D. plexippus. Further research is needed to assess the likelihood of D. plexippus exposure to H. axyridis in the field and to quantify the likelihood of H. axyridis having an adverse effect on D. plexippus in the presence of other prey, particularly aphids. These data could be used to develop an ecological risk assessment.

Toxicity of commonly used insecticides in sweet corn and soybean to multicolored asian lady beetle (Coleoptera: Coccinellidae)

Abstract Use of insecticides with low toxicity to natural enemies is an important component of conservation biological control. In this study, we evaluated the toxicity of insecticides used in sweet corn, Zea mays L., and soybean, Glycine max (L.) Merr., to the multicolored Asian lady beetle, Harmonia axyridis (Pallas), under laboratory and field conditions. Field experiments conducted in sweet corn in 2003 and 2004 and in soybean in 2003, showed that H. axyridis was the most abundant predator. In sweet corn, densities of H. axyridis larvae in plots treated with spinosad or indoxacarb were generally higher than in plots treated with chlorpyrifos, carbaryl, bifenthrin, and λ-cyhalothrin. In soybean, densities of H. axyridis larvae in plots treated with chlorpyrifos were higher than in plots treated with λ-cyhalothrin. Laboratory experiments were conducted to evaluate the acute toxicity of insecticides to eggs, first and third instars, pupae, and adults. Spinosad, followed by indoxacarb, were the least toxic insecticides for all life stages of H. axyridis. Conventional insecticides showed high toxicity to H. axyridis when applied at field rates under laboratory conditions. Overall, first instars were most susceptible to the insecticides tested, followed by third instars and adults, eggs, and pupae. Our results suggest that spinosad, and to a lesser extent indoxacarb, offer reduced toxicity to H. axyridis and would be beneficial for conservation biological control in agricultural systems where H. axyridis is abundant.

Cold Hardiness of the Multicolored Asian Lady Beetle (Coleoptera: Coccinellidae)

Abstract A classical biological control agent, Harmonia axyridis (Pallas), is having both beneficial and detrimental impacts in North America. The objective of this study was to evaluate the cold hardiness of H. axyridis in North America. Supercooling points and survival at subzero temperatures of field-collected and insectary-reared H. axyridis were examined. The mean (±SE) supercooling points for eggs and pupae (i.e., nonfeeding stages) were −27.0 ± 0.18°C and −21.3 ± 0.52°C, respectively. The mean supercooling points for larvae and adults (i.e., feeding stages) were −14.17 ± 0.33 and −11.9 ± 0.53°C, respectively. Sex and color morph (i.e., red: f. succinea versus black: f. spectabilis) had no effect on the supercooling point of H. axyridis adults. Mean supercooling points of H. axyridis adults from Minnesota and Georgia were significantly lower during winter months than summer months. The mortality of H. axyridis increased significantly after individuals were exposed to temperatures below the mean supercooling point of the population. Supercooling point was a good predictor of cold hardiness. However, the cold hardiness of H. axyridis appears to be a poor predictor of its northern distribution.

Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis.

Inferences about introduction histories of invasive species remain challenging because of the stochastic demographic processes involved. Approximate Bayesian computation (ABC) can help to overcome these problems, but such method requires a prior understanding of population structure over the study area, necessitating the use of alternative methods and an intense sampling design. In this study, we made inferences about the worldwide invasion history of the ladybird Harmonia axyridis by various population genetics statistical methods, using a large set of sampling sites distributed over most of the species’ native and invaded areas. We evaluated the complementarity of the statistical methods and the consequences of using different sets of site samples for ABC inferences. We found that the H. axyridis invasion has involved two bridgehead invasive populations in North America, which have served as the source populations for at least six independent introductions into other continents. We also identified several situations of genetic admixture between differentiated sources. Our results highlight the importance of coupling ABC methods with more traditional statistical approaches. We found that the choice of site samples could affect the conclusions of ABC analyses comparing possible scenarios. Approaches involving independent ABC analyses on several sample sets constitute a sensible solution, complementary to standard quality controls based on the analysis of pseudo‐observed data sets, to minimize erroneous conclusions. This study provides biologists without expertise in this area with detailed methodological and conceptual guidelines for making inferences about invasion routes when dealing with a large number of sampling sites and complex population genetic structures.

A Simple Method for In-Field Sex Determination of the Multicolored Asian Lady Beetle Harmonia axyridis

Abstract The multicolored Asian lady beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), has become a popular study organism due to its promise as a biological control agent and its potential adverse, non-target impacts. Behavioral and ecological research on H. axyridis, including examinations of its impacts, could benefit from non-destructive or non-disruptive sexing techniques for this coccinellid. External morphological characters were evaluated for H. axyridis (succinea color form) sex determination in laboratory and field studies. The shape of the distal margin of the fifth visible abdominal sternite accurately predicted H. axyridis sex for all beetles examined. Males consistently had a concave distal margin, while females had a convex distal margin. In addition, pigmentation of the labrum and prosternum were both significantly associated with H. axyridis sex; males had light pigmentation and females had dark pigmentation. Labrum and prosternum pigmentation increased from light to dark with decreasing rearing temperature and increasing time after adult eclosion for females. Male pigmentation was only affected by a decrease in rearing temperature. Validation through in-field collections indicated that these predictors were accurate. However, labrum pigmentation is a more desirable character to use to determine sex, because it is more accurate and easily accessible. Therefore, we recommend using labrum pigmentation for in-field sex determination of H. axyridis. Implications of this diagnostic technique for applied and basic research on this natural enemy are discussed.

Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America

In summer 2007, the Asian parasitoid Binodoxys communis (Hymenoptera: Braconidae) was released in North America for control of the exotic soybean aphid, Aphis glycines (Hemiptera: Aphididae). Despite its comparatively narrow host range, releases of B. communis may still constitute a risk to native aphid species. To estimate the risk of exposure of non-target aphids to B. communis, we merged assessments of temporal co-occurrence with projections of spatial overlap between B. communis and three native aphid species, and in-field measurements of the incidence of ecological filters that may protect these aphids from parasitism. Temporal co-occurrence was assessed between A. glycines and native aphids (Aphis asclepiadis, Aphis oestlundi, and Aphis monardae) at four different locations in Minnesota, USA. The degree of temporal overlap depended greatly on location and aphid species, ranging between 0 and 100%. All of the native aphids were tended by multiple species of ants, with overall ant-attendance ranging from 26.1 to 89.6%. During temporal overlap with A. glycines, 53 ± 11% of A. monardae colonies were partly found in flower heads of their host plant, with flowers acting as a physical refuge for this aphid. The extent of geographic overlap between B. communis and native aphids based upon Climex modeling was 17–28% for A. monardae, 13–22% for A. oestlundi, 46–55% for A. asclepiadis and 12–24% for the A. asclepiadis species complex. The estimated overall probability of potential exposure of B. communis on native aphids was relatively low (P = 0.115) for A. oestlundi and high (P = 0.550) for A. asclepiades. Physical and ant-mediated refuges considerably lowered probability of population-level impact on A. monardae, and could lead to substantial reduction of exposure for the other native aphids. These findings are used to make broader statements regarding the ecological safety of current B. communis releases and their potential impact on native aphid species in North America.

Impact of fruit feeding on overwintering survival of the multicolored Asian lady beetle, and the ability of this insect and paper wasps to injure wine grape berries

The establishment of the multicolored Asian lady beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in North America has resulted in negative impacts on fruit production. We investigated the overwintering survival of H. axyridis after feeding on four diets: injured wine grape berries, 25% sucrose solution, water, and a control containing no food or water. After being exposed to these diets for 6 days, live individuals were transferred to clean plastic Petri dishes, and held at 5 ± 1 °C in growth chambers throughout the winter. Survival was recorded every month. Adult lady beetles collected during the overwintering flight in mid‐October had higher survival rates than beetles collected from soybean fields in mid‐August. These results suggest that an adaptation period prior to diapause increases the chances of lady beetle survival over the winter. In addition, injured wine grape berries, sugar, and water decreased beetle mortality during the overwintering months. Our results also showed that under similar conditions, females have higher survival during the winter than males. The importance of sugar and water on winter survival may drive H. axyridis adults to vineyards for feeding on wine grapes. Finally, we tested if adults of H. axyridis and the European paper wasp, Polistes dominulus Christ (Hymenoptera: Vespidae), were able to break the grape skin. Harmonia axyridis adults and paper wasps were not able to cause the primary injury to berries of Frontenac grapes under laboratory conditions. These results suggest that control of paper wasps in vineyards may not affect H. axyridis aggregations, and that H. axyridis feeding on wine grapes depends on previous injury to grape berries.

Influence of Alternate Prey on Predation of Monarch Butterfly (Lepidoptera: Nymphalidae) Larvae by the Multicolored Asian Lady Beetle (Coleoptera: Coccinellidae)

Abstract An invasive, exotic coccinellid, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), was recently identified as a potential hazard to immature monarch butterflies, Danaus plexippus L. (Lepidoptera: Nymphalidae). To further evaluate the risk of H. axyridis impacting D. plexippus, we evaluated the influence of an alternate prey, Aphis nerii Boyer de Fonscolombe (Homoptera: Aphididae), on the predation rate of H. axyridis on D. plexippus larvae. When first-instar D. plexippus were placed in petri dish arenas with third-instar H. axyridis and varying densities of A. nerii, D. plexippus survival after 24 h increased significantly from 0% with 0 A. nerii present to 73% with 30 A. nerii present. In predation studies conducted in field cages, survival of D. plexippus larvae decreased with increasing densities of H. axyridis larvae and tended to increase with increasing A. nerii densities. These studies indicate that H. axyridis will feed on D. plexippus larvae in the presence of A. nerii, but that the presence of A. nerii lessens the severity of predation on D. plexippus.