Asian Lady Beetle Harmonia Axyridis Research Articles

EXPANSION OF <i>HARMONIA AXYRIDIS</i> (PALLAS, 1773) (COLEOPTERA: COCCINELLIDAE) IN THE EUROPEAN PART OF RUSSIA IS CONTINUING

In the European part of Russia, the first records of multicoloured Asian ladybird Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) were observed in 2004 from the territory of the Belgorod Region. In recent years (2018-2020) H. axyridis has quickly spread across the Volga Region and the center of European Russia, and this expansion is continuing. In 2021-2022 H. axyridis was recorded in Saint-Petersburg, Leningrad, Sverdlovsk, Vologda Regions and Mari El Republic for the first time. The findings of H. axyridis from Ekaterinburg are the first record for Trans-Urals territory and the easternmost locality known in invasive (European) part of the species range.

Consumption patterns of the multicolored Asian ladybird Harmonia axyridis on the broad bean aphid Aphis craccivora

• Consumption patterns of ladybirds is meaningful for biological control programs. • Ladybird females were superior predator of aphids base on functional response. • Fourth-instar ladybird larvae suffered from greater intraspecific competition. • Adults and 4th-instar larvae of ladybirds are more effective in controlling aphids. • Intraspecific competition should be considered during field releases of ladybirds. The multicolored Asian ladybird Harmonia axyridis Pallas is often used as a biological control agent against Aphis craccivora Koch, a key pest aphid of broad bean. Understanding consumption characteristics of biological control agents is critical for developing effective biological control programs. Here, under laboratory conditions we studied consumption patterns of H. axyridis on A. craccivora including functional response and intraspecific competition. All larvae (1st-, 2nd-, 3rd-, 4th-instar) and adults (male and female) of H. axyridis exhibited a Type II functional response to A. craccivora . We found H. axyridis females were superior to individuals of other developmental stages, based on three key parameters in functional response model, i.e. attack rate ( a = 90.0%), handling time ( T h = 2.7 min), and consumption threshold ( N max = 526.7 individuals). Results from our analysis of intraspecific competition showed that when attacking A. craccivora , 4th-instar larvae of H. axyridis suffered from the greatest intraspecific competition (coefficient of mutual interference, m = 0.48). Our results show that 4th-instar larvae and adults of H. axyridis are most effective in controlling A. craccivora , and proper density of H. axyridis released will reduce intraspecific competition. This analysis reveals both prey-predator and predator-predator interactions, and highlights the value of biological control in reducing pesticide use and protecting ecological environments.

Molecular identification of the Asian lady beetle Harmonia axyridis in Israel

Molecular identification of the Asian lady beetle Harmonia axyridis in Israel

Life tables of the ladybird beetles Harmonia axyridis, Cycloneda sanguinea and Hippodamia convergens reared on the greenbug Schizaphis graminum.

The Asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae) is a biological control agent that also may adversely impact other coccinellid species. Life table parameters were used to assess the population growth potential and the effects of interspecific competition between the invasive lady beetle H. axyridis and the native coccinellids Hippodamia convergens and Cycloneda sanguinea (Coleoptera: Coccinellidae) under laboratory conditions at 25 °C, using Schizaphis graminum (Hemiptera: Aphididae) as prey. The effects of the abiotic factors air temperature and humidity on these coccinellids by conducting a survey in a sorghum crop under average conditions of 18.1 °C and 53.5%, respectively, were also assessed. Fecundity was higher in C. sanguinea (1021.0 eggs per female) and H. axyridis (1029.2 eggs per female) than in H. convergens (484.5 eggs per female). The majority of the life table parameters showed no significant differences. The instantaneous rates of population increase (rm) of C. sanguinea, H. axyridis, and H. convergens were 0.195, 0.198, and 0.194 d-1, respectively. Based on the life table parameters obtained in this study, all three species of Coccinellidae showed a similar capacity to control a S. graminum population.

<i>HARMONIA AXYRIDIS</i> (PALLAS, 1773) (COLEOPTERA: COCCINELLIDAE) IN MOSCOW CITY AND YALTA CITY: ITS COMPETITION WITH NATIVE SPECIES OF COCCINELLIDS AND THE INFLUENCE OF PARASITOIDS ON ITS NUMBER

The Asian ladybird Harmonia axyridis is an invasive species that is rapidly spreading around the world. Occupying new territories, H. axyridis often causes a decrease in the biodiversity of native species of coccinellids, competing with them for food resources. A comparison of H. axyridis with six species of ladybirds was made in terms of the ratio of the number of individuals and the degree of infestation with parasitoids. In Moscow city, the most widespread species of ladybirds was Adalia bipunctata (67.1%), H. axyridis ranks second (16.5%). The total infestation of H. axyridis pupae with parasitoids is 1.8% in Moscow city and 12.2% in Yalta city. Infestation with parasitoids of other ladybird species in Moscow city is much higher: from 11.0% to 36.4%. Thus, parasitoids effectively regulate the number of native ladybird species, but have an insignificant effect on the number of the invasive species H. axyridis .

Invasion of the Asian Ladybird Harmonia axyridis (Pallas, 1773) in the European Part of Russia

The natural range of the Asian ladybird Harmonia axyridis (Pallas, 1773) covers the territories of China, Mongolia, Korea, Japan, and Russia (Far East, Southern Siberia, and Altai). Since the early 1980's, the global invasion of H. axyridis began, first on the territory of the United States, from where the Asian ladybird spread to South America, Africa, and Europe. By 2016, this species occupied all of Western Europe with the exception of its northern and southern regions. Penetration of H. axyridis on the territory of the Russian Federation (Kaliningrad) was discovered in 2010, and since 2011, the species has spread to the Black Sea coast. This report presents our data on the distribution of Harmonia axyridis in central Russia, from its western borders, to the Volga River. The occupation of this huge territory by this species occurred mainly in the last 3 years−2018–2020. The rate of movement of the species on the territory of the European part of Russia is about 200 km/year.

Key role of juvenile hormone in controlling reproductive diapause in females of the Asian lady beetle Harmonia axyridis.

The Asian lady beetle Harmonia axyridis is an important predator of several agricultural pests, including aphids and whiteflies, and thus can contribute to pest management. Commercial viability as a pest control method requires that the beetle can be mass-reared, and that workable conditions for extended shelf-life can be guaranteed. One of the features of Harmonia's life cycle is that it enters diapause in the adult stage when the length of the photophase starts shortening in late summer. Reduction of juvenile hormone (JH) titer has been demonstrated to be the common endocrine mechanism inducing reproductive diapause in insects. However, whether H. axyridis enters diapause dependent on JH shutdown and how the JH level is regulated before diapause remains unknown. Like in other insects, the absence of JH triggers the induction and maintenance of reproductive diapause in H. axyridis, indicated by JH measurements and the knockdown of an intracellular JH receptor methoprene-tolerant (Met). Methoprene, a JH analog, significantly reversed diapause into reproduction via Met. Combined with RNA-sequencing and RNA interference, we also demonstrated that JH biosynthesis rather than the JH degradation pathway determines the reduction of JH titer in diapausing females. Our results reveal the vital role of JH in regulating reproductive diapause in female H. axyridis. Harmonia axyridis diapause could thus be manipulated by targeting JH production and JH signaling. © 2021 Society of Chemical Industry.

Comparative Study of the Phenotypic Structure and Photoperiodic Responses of Female Asian Ladybirds Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) from Moscow, Belgorod, and Sochi

Insect invasions are often accompanied by changes in the phenotypic structure of the populations and in the photoperiodic responses that regulate seasonal cycles. The Asian ladybird Harmonia axyridis has been recently discovered in Krasnodar Territory, from whence it is now gradually colonizing Central Russia. Our comparative study of individuals collected in 2020 in Sochi, Belgorod Province, and Moscow Province shows that interpopulation differences in their phenotypic structure are nonsignificant. The proportion of the light morph succinea is 77–83%; the proportion of the most common dark morph, spectabilis, is 13–20%. Laboratory experiments show that females from all the studied populations exhibit only a weak photoperiodic response. Comparative analysis reveals that females from the more northerly Moscow and Belgorod populations have a somewhat greater tendency to diapause and slightly delay reproductive maturation.

The impacts of Harmonia axyridis cues on foraging behavior of Aphidius gifuensis to Myzus persicae

This study investigated the effect of adult associated cues of the multicolored Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on the foraging behavior of the aphid parasitoid, Aphidius gifuensis Ashmead (Hymenoptera: Aphididae) with three assays: 1) whole aphid leaf-disc with H. axyridis tracks; 2) aphid leaf-disc with only half contaminated with H. axyridis tracks; 3) aphid leaf-discs without H. axyridis tracks. Foraging behavior of A. gifuensis was recorded using the Observer® XT 11 and EthoVsion® XT 12. In addition, functional responses of A. gifuensis in patches with or without H. axyridis cues were also tested. Aphidius gifuensis females preferred oviposition in arenas where no adult tracks of H. axyridis were present. However, no significant difference between functional responses of A. gifuensis foraging in plants with and without H. axyridis cues was detected. Our study suggests that H. axyridis associated cues could influence the foraging behavior and activity of A. gifuensis under laboratory conditions. On the other hand, the foraging efficiency of A. gifuensis was not significantly affected by H. axyridis walking tracks in a single plant system. Aphidius gifuensis might exhibit flexible behavioral responses to predator associated cues. The risk of intraguild interactions and the possibility of mitigating such risks for parasitoids are important components for ultimately determining the compatibility of biological control agents.

The First Record of the Alien Ladybug Harmonia axyridis Pall. 1773 (Coleoptera, Coccinellidae) in Azerbaijan

For the first time, data on the invasion of the Asian lady beetle Harmonia axyridis (Pallas, 1773) in Azerbaijan are presented. At the end of March 2019, two specimens of H. axyridis were collected in the forests formed by the trees of Parrotia persica (DC.) C.A. Mey near the border with Iran on the territory of the Hyrcanian National Park. The native range of the species includes the southeast of Western Siberia, the south of Eastern Siberia and the Far East, Northeastern Kazakhstan, Mongolia, China, the Korean Peninsula, Japan, and Northern Vietnam. Now it is expanding worldwide. At the moment, H. axyridis is found in more than 50 countries in Europe, Asia, Africa, and North and South America. The finding of the species in Azerbaijan shows that its invasion in the region continues.

Aspartate-β-alanine-NBAD pathway regulates pupal melanin pigmentation plasticity of ladybird Harmonia axyridis.

Phenotypic plasticity is observed in many animal species and it is effective for them to cope with many types of environmental threats. The multicolored Asian ladybird Harmonia axyridis shows a cuticular pigmentation plasticity that can be rapidly induced by temperature changes, and in the form of changeable melanin spot patterns to adjust heat-absorbing. Here, H. axyridis with thermal stimulation were selected for determining the molecular regulations behind it. First, we confirmed the melanin level changes of H. axyridis pupa could be induced by temperature, and then screened the efficient time window for thermal sensing of H. axyridis pre-pupa; it is suggested that the late stage of pre-pupa (late stage of 4th instar larva) is the critical period to sense thermal signals and adjust its pupal melanin spot area size to adapt to upcoming thermal conditions. The Ha-ADC (aspartate decarboxylase) and Ha-ebony (NBAD synthase) of aspartate-β-alanine-NBAD pathway were then proved in regulation of cuticular melanization for pupa through RNA interference experiments; knockdown of these two genes enlarged the melanin spot size. Finally, we designed a random injection of Ha-ADC at different pre-pupal stages, to further study the regulation window during this process. Combined with all evidence observed, we suggested the spot size determination can be regulated very close to the time point of pupation, and genes of the aspartate-β-alanine-NBAD pathway play an important role at the molecular level. In brief, H. axyridis exhibits a flexible active physiological regulation through transcriptional modification to thermal changes.

Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe

While detrimental effects of invasive predators on native species are well documented, we often lack a mechanistic understanding of the invasion success. Lack of prey avoidance behaviour can lead to higher consumption rates by invasive predators compared to native predators. This competitive advantage is expected to contribute to the invasion success of non‐native predators. We compared aphid consumption and cue avoidance behaviour of aphids between four native ladybird species (Coccinella septempunctata, Adalia bipunctata, Propylea quatuordecimpunctata, and Hippodamia variegata) and the invasive Asian ladybird Harmonia axyridis. The invasive H. axyridis and the native C. septempunctata consumed more aphids than the three smaller native ladybird species. In line with our expectations, aphids avoided leaves bearing cues of most native ladybird species but not of the invasive H. axyridis. Our results indicate that body size rather than ladybird origin determined aphid predation rates. The lack of aphid avoidance behaviour towards cues of H. axyridis indicates that they were not able to recognise the chemical cues of the invasive predator. Relatively large body size and the absence of cue avoidance in aphids might benefit the invasive H. axyridis, particularly in comparison to smaller native ladybird species. The absence of avoidance behaviour in aphids might lead to even higher predation rates of H. axyridis under more natural conditions.

Lethal and Sublethal Effects of Chlorpyrifos on Biological Traits and Feeding of the Aphidophagous Predator Harmonia axyridis.

Except of pest control, insecticides have shown adverse effects on natural enemies as well. Thus, risk assessment of pesticides for biological control agents is critical for effective use in integrated pest management (IPM) schemes. In the present study, the lethal and sublethal effects of chlorpyrifos, a commonly used insecticide that may negatively affect biological control agents, were evaluated on a non-target predator, the Asian ladybeetle Harmonia axyridis. Previous studies have reported on lethal concentrations, but the effects of sublethal concentrations remain unclear. Lethal and sublethal concentrations of chlorpyrifos were applied to third instar larvae of H. axyridis, and different growth and developmental parameters were measured. Treatment with LC10 (4.62 mg a.i. L−1) significantly shortened the developmental period of third instar larvae, whereas it significantly prolonged those of fourth instar larvae and pupa. Treatment with LC30 (9.59 mg a.i. L−1) significantly increased the larval and pupal developmental period compared with that of the control, whereas feeding potential, female fecundity, and adult longevity significantly decreased after LC10 and LC30 treatment. The pre-oviposition period significantly increased compared with that of the control. Population growth parameters, the finite (λ) and intrinsic rate of increase (r) and the net reproductive rate (R0), decreased following exposure to sublethal concentrations of chlorpyrifos. According to the results, the use of chlorpyrifos in IPM schemes requires further research because even sublethal concentrations of this insecticide were harmful to H. axyridis population growth.

Effects of pterostigma structure on vibrational characteristics during flight of Asian ladybird Harmonia axyridis (Coleoptera: Coccinellidae)

The hind wings of beetles are deployable and play an essential role in flight. In the Asian ladybird Harmonia axyridis (Coleoptera: Coccinellidae), the pterostigma (pst) is found in the middle of the hind wing instead of at the tip of the hind wing. This paper investigates the effect of the pst on the vibrational characteristics during the flight of H. axyridis. Based on cross sections of the pst and veins as well as the morphology and nanomechanical properties of the hind wing, including the wing membrane and veins, three three-dimensional coupling models, Models I–III, of hind wings with/without pst structures and veins with varying or uniform reduced moduli are established. Modal analysis results for these three models show that the vibrational characteristics and deformation tendencies change the flight performance of the hind wing models with pst structures compared with that of the other models. The results in this paper reveal that the pst structure has an important influence on vibrational characteristics and deformation tendencies and, hence, on flight performance; the relationships between the body mass and the area of the hind wing, which have significant implications for the design of biomimetic deployable wing structures for micro air vehicles (MAVs), are also analyzed.

Comparative Assessment of Genetic Structure in Invasive and Autochthonous Populations of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae)

The genetic diversity of two native Siberian and two invasive European populations of the Asian ladybird Harmonia axyridis was studied under laboratory conditions. Analysis of the population genetic structure revealed a high degree of isolation of the monomorphic population from Sochi, monomorphism of the population from Serbia, and high genetic heterogeneity of the populations from Novosibirsk and Altai. The allelic profile data showed that the Novosibirsk population contained the greatest number of alleles. Our preliminary results indicate high genetic homogeneity of the Sochi population, which is consistent with the initial stage of expansion and contradicts the hypothesis of its hybrid origin.

Concentration and distribution of diaphorin, and expression of diaphorin synthesis genes during Asian citrus psyllid development

The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Sternorrhyncha: Psylloidea: Liviidae) is an important pest of citrus species worldwide because it transmits Candidatus Liberibacter spp. (Alphaproteobacteria); the causative agents of an incurable citrus disease known as huanglongbing or greening disease. D. citri possesses a vertically transmitted intracellular symbiont, Candidatus Profftella armatura (Betaproteobacteria), which produces diaphorin; a polyketide that is toxic to various eukaryotic organisms. Our previous study demonstrated that the total amount and average concentration of diaphorin in adult D. citri, when homogeneous distribution is assumed within the insect, are sufficient to exert inhibitory effects on fungi and insects, including the Asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae); one of the major predators of D. citri. However, diaphorin may be localized to a limited body area within D. citri, and its concentration may change during development. In the present study, to better understand the physiological and ecological function of diaphorin, we assessed the distribution of diaphorin within the D. citri body and analyzed concentrations of diaphorin in various developmental stages. Expression of genes involved in diaphorin synthesis was also analyzed. The results demonstrated that diaphorin is distributed widely in the D. citri body, which appears to be a prerequisite for effective deterrence of natural enemies. The concentration of diaphorin was shown to change significantly during the development of D. citri. It was highest in mature adults, followed by embryos and teneral adults, and lowest in nymphs. The lowest concentrations of diaphorin observed in nymphs are still presumed to be effective in deterring invasive natural enemies, including parasites, parasitoids, and entomopathogenic fungi. Quantitative RT-PCR indicated that amounts of transcripts for diaphorin synthesis genes dipP and dipT were at a minimum in embryos, increased during the nymphal period, and reached a maximum level just after adult eclosion. The alteration pattern of the amounts of transcripts for diaphorin synthesis genes appeared to partially disagree with that of the concentration of diaphorin. The present study provides new insights into the function of diaphorin, which is essential for further investigations that aim to improve the efficacy of D. citri biological control.

Diaphorin, a polyketide synthesized by an intracellular symbiont of the Asian citrus psyllid, is potentially harmful for biological control agents.

The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Sternorrhyncha: Psylloidea: Liviidae) is an important pest of citrus species worldwide because it transmits Candidatus Liberibacter spp. (Alphaproteobacteria), the causative agents of an incurable citrus disease known as huanglongbing or greening disease. Diaphorina citri possesses a vertically-transmitted intracellular symbiont, Candidatus Profftella armatura (Betaproteobacteria), which produces diaphorin, a polyketide that is significantly toxic to mammalian cells. Diaphorin is an analog of pederin, a defensive polyketide in the body fluid of Paederus rove beetles (Coleoptera: Staphylinidae) that deters predators. In the present study, as a first step to assess the possibility that diaphorin is toxic to biological control agents, we assayed diaphorin activities against insects and fungi. The target cells and organisms were (a) the Sf9 cell line derived from the fall armyworm moth Spodoptera frugiperda (Lepidoptera: Noctuidae), (b) the pea aphid Acyrthosiphon pisum (Hemiptera: Sternorrhyncha: Aphidoidea: Aphididae), a phloem sap-sucking insect that is closely related to psyllids, (c) the Asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae), one of the major predators of D. citri, and (d) the budding yeast Saccharomyces cerevisiae (Ascomycota: Saccharomycetes) as a model of fungal pathogens. For a comparison, we also evaluated pederin activities. The results of our analyses revealed the following: (1) Diaphorin and pederin are significantly toxic to the tested insects and yeast; (2) Their toxicities vary widely among the target cells and organisms; (3) Diaphorin is generally less toxic than pederin; (4) The toxicities of diaphorin and pederin are considerably different in the Sf9 insect cell line and S. cerevisiae, but similar in A. pisum and H. axyridis; and (5) The amount of diaphorin contained in D. citri is toxic to all of the tested cells and organisms, suggesting that this polyketide is potentially harmful for biological control agents.

The taste of origin in a lady beetle: do males discriminate between females based on cuticular hydrocarbons?

AbstractThe Asian lady beetle Harmonia axyridis originates from Asia and has established invasive populations worldwide. Recent population genetic studies trace their invasion routes and demonstrate that bottlenecks in population size have reduced their genetic diversity. Consequently, phenotypical differences are highlighted between native and invasive populations. Among phenotypical traits, cuticular hydrocarbons (CHCs) might reflect the geographical origin of a lady beetle, especially because of their genetic basis. The present study investigates whether (i) the CHC profiles qualitatively and quantitatively differ between females of H. axyridis from native and invasive populations and (ii) males discriminate females from native and invasive populations using CHC profiles. CHCs are solvent‐extracted before being quantified and identified by gas chromatography and mass spectrometry. In total, 17 CHCs are detected from female elytra, including six alkanes, three polyunsaturated and eight monounsaturated alkenes. The total quantity of CHCs differs among the populations, with lady beetles from Tai'an (China) displaying higher CHC concentrations than lady beetles from Gembloux (Belgium) and from Beijing (China) populations. Multivariate analyses detect differences in CHC qualitative profiles, with females from Tai'an being different from the two other populations. Finally, behavioural assays show that females originating from the native Tai'an population are less preferred by males, whereas females from the invasive population are mounted more often. The behavioural assays suggest that CHCs are not involved in discrimination of mating partners based on their origin.

Occurrence of the Invasive Lady Beetle Harmonia Axyridis (Pallas) (Coleoptera: Coccinellidae) in Iran

The Asian lady beetle Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is one of the most invasive insects worldwide. It has been introduced into several continents for classical biological control and by accident. The current study is the first report of this species from Iran (new country record). All developmental stages and adults of two morphs, succinea and spectabilis, were collected from fruit trees and ornamental gardens in the city of Rasht in the northern Iranian province Guilan in 2016. We collected 249 adults of the color morph succinea and 31 individuals (11%) of the melanic color morph spectabilis. Only 36% of individuals were males. Larvae and pupae were found from April to September, adults from April to October.

Volatiles from aphid-infested plants attract adults of the multicolored Asian lady beetle Harmonia axyridis

Volatiles play important roles in the recruitment of arthropod natural enemies, and are widely used in foraging by the multicolored Asian lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae). In its native range in Asia and throughout its invaded range, H. axyridis preys upon multiple species of aphids in both natural and agricultural settings, yet little is known about the volatile cues it employs to locate prey items. In this study, we test the attractiveness of volatiles emanating from four different aphid × plant combinations to H. axyridis adults in a Y-tube olfactometer. More specifically, we exposed host plants from various plant families as such: Artemisia lavandulaefolia (Asteraceae) with Macrosiphoniella artemisiae; Gossypium hirsutum (Malvaceae) with Aphis gossypii; Triticum aestivum (Poaceae) with Sitobion avenae and Schizaphis graminum; and Vicia faba (Fabaceae) with Megoura viciae. Next, using coupled gas chromatography – electroantennogram detection (GC-EAD) and gas chromatography – mass spectrometry (GC-MS), we identified the volatile compounds from aphid × plant combinations that elicit electrophysiological activity in H. axyridis adults. Lastly, a total of five volatiles were assessed in open-field tests with barrel traps. In olfactometer assays, H. axyridis adults preferred aphid-infested plants over un-infested plants or aphids alone. In GC-EAD trials, seven electrophysiologically-active compounds were found; and in ensuing behavioral assays, ladybeetles preferred five kinds of volatiles (i.e., p-diethylbenzene, 3-ethylacetophenone, 1,2-diethylbenzene, α-pinene and butyl acrylate). In open-field tests, H. axyridis were significantly attracted to all five info-chemicals at a concentration 100 mg/ml. Our work not only sheds light upon H. axyridis chemical ecology, but equally provides important information that can facilitate the future development of integrated pest management (IPM) tactics for aphid control or volatile-based trapping and monitoring technologies for H. axyridis in its invaded range.