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Concept: Harmonia axyridis

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The harlequin ladybird beetle Harmonia axyridis has emerged as a model species in invasion biology because of its strong resistance against pathogens and remarkable capacity to outcompete native ladybirds. The invasive success of the species may reflect its well-adapted immune system, a hypothesis we tested by analysing the transcriptome and characterizing the immune gene repertoire of untreated beetles and those challenged with bacteria and fungi. We found that most H. axyridis immunity-related genes were similar in diversity to their counterparts in the reference beetle Tribolium castaneum, but there was an unprecedented expansion among genes encoding antimicrobial peptides and proteins (AMPs). We identified more than 50 putative AMPs belonging to seven different gene families, and many of the corresponding genes were shown by quantitative real-time RT-PCR to be induced in the immune-stimulated beetles. AMPs with the highest induction ratio in the challenged beetles were shown to demonstrate broad and potent activity against Gram-negative bacteria and entomopathogenic fungi. The invasive success of H. axyridis can therefore be attributed at least in part to the greater efficiency of its immune system, particularly the expansion of AMP gene families and their induction in response to pathogens.

Concepts: Immune system, Gene, Bacteria, Evolution, Biology, Beetle, Coccinellidae, Harmonia axyridis

176

Harmonia axyridis has been introduced as a biological control agent in Europe and the USA. Since its introduction, it has established and spread, and it is now regarded as an invasive alien species. It has been suggested that intraguild predation is especially important for the invasion success of H. axyridis. The aim of this study was to compare the intraguild predation behaviour of three ladybird species (Coccinella septempunctata, Adalia bipunctata, and H. axyridis). Predation behaviour was investigated in semi-field experiments on small lime trees (Tilia platyphyllos). Two fourth-instar larvae placed on a tree rarely made contact during 3-hour observations. When placed together on a single leaf in 23%-43% of the observations at least one contact was made. Of those contacts 0%-27% resulted in an attack. Harmonia axyridis attacked mostly heterospecifics, while A. bipunctata and C. septempunctata attacked heterospecifics as often as conspecifics. In comparison with A. bipunctata and C. septempunctata, H. axyridis was the most successful intraguild predator as it won 86% and 44% of heterospecific battles against A. bipunctata and C. septempunctata respectively, whilst A. bipunctata won none of the heterospecific battles and C. septempunctata won only the heterospecific battles against A. bipunctata. Coccinella septempunctata dropped from a leaf earlier and more often than the other two species but was in some cases able to return to the tree, especially under cloudy conditions. The frequency with which a species dropped did not depend on the species the larva was paired with. The results of these semi-field experiments confirm that H. axyridis is a strong intraguild predator as a consequence of its aggressiveness and good defence against predation from heterospecific species. The fact that H. axyridis is such a strong intraguild predator helps to explain its successful establishment as invasive alien species in Europe and the USA.

Concepts: Biological pest control, Invasive species, Introduced species, Coccinellidae, Harmonia axyridis, Tilia, Coccinella septempunctata, Biological pest control agents

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The harlequin ladybird, Harmonia axyridis, has emerged as a model species for invasion biology, reflecting its remarkable capacity to outcompete native ladybird species when introduced into new habitats. This ability may be associated with its prominent resistance to pathogens and intraguild predation. We recently showed that the constitutive antibacterial activity present in the haemolymph of H. axyridis beetles can be attributed to the chemical defence compound harmonine. Here, we demonstrate that H. axyridis differs from other insects, including the native ladybird Coccinella septempunctata, by reducing rather than increasing the antimicrobial activity of its haemolymph following the injection of bacteria. However, both species produce new or more abundant proteins in the haemolymph, indicating that bacterial challenge induces innate immune responses associated with the synthesis of immunity-related proteins. Our results suggest that H. axyridis beetles can switch from constitutive chemical defence to inducible innate immune responses, supporting hypothesis that inducible antimicrobial peptides protect host beetles against pathogens that survive constitutive defences. These alternative antimicrobial defence mechanisms may reflect a trade-off resulting from fitness-related costs associated with the simultaneous synthesis of harmonine and antimicrobial peptides/proteins.

Concepts: Immune system, Bacteria, Microbiology, Innate immune system, Coccinellidae, Harmonia axyridis, Coccinella septempunctata, Biological pest control agents

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Invasive species that proliferate after colonizing new habitats have a negative environmental and economic impact. The reason why some species become successful invaders, whereas others, even closely related species, remain noninvasive is often unclear. The harlequin ladybird Harmonia axyridis, introduced for biological pest control, has become an invader that is outcompeting indigenous ladybird species in many countries. Here, we show that Harmonia carries abundant spores of obligate parasitic microsporidia closely related to Nosema thompsoni. These microsporidia, while not harming the carrier Harmonia, are lethal pathogens for the native ladybird Coccinella septempunctata. We propose that intraguild predation, representing a major selective force among competing ladybird species, causes the infection and ultimate death of native ladybirds when they feed on microsporidia-contaminated Harmonia eggs or larvae.

Concepts: Ecology, Invasive species, Introduced species, Coccinellidae, Harmonia axyridis, Coccinella septempunctata, Biological pest control agents, Coccinella

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Ladybug taint (LBT) is a wine fault caused by the inadvertent incorporation of ladybeetles to the wine during the winemaking process. Harmonia axyridis, also known as the multicolored Asian lady-beetle (MALB), was the only species considered responsible for causing the taint. A second species, Coccinella septempunctata (7 Spot), has recently also been implicated. The main objectives of this study were to identify and quantify the compounds associated with ladybug taint of white and red wine from these two Coccinellidae species (Harmonia axyridis and Coccinella septempunctata), and determine the most odor-active compounds in LBT-affected wines.

Concepts: Wine, Oenology, Acids in wine, Coccinellidae, Harmonia axyridis, Coccinella septempunctata, Biological pest control agents, Coccinella

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The cowpea aphid Aphis craccivora that infests the black locust Robinia pseudoacacia shows toxicity to its predator, the multicolored Asian ladybird beetle, Harmonia axyridis. In contrast, the same aphid species that infests the common vetch, Vicia angustifolia, is suitable prey for H. axyridis larvae. Previously, it was reported that the toxicity of A. craccivora infesting R. pseudoacacia was due to canavanine and 2-aminoethanol, but there was some doubt about the toxicity of these compounds and their concentrations in the aphids. In the present study, we determined the concentrations of cyanamide, canavanine, and 2-aminoethanol in A. craccivora infesting the two host plants. In the extracts of A. craccivora that infested either of the host plants, canavanine was undetectable, and 2-aminoethanol was detected at the concentration of 3.0-4.0 μg/g fresh weight. Cyanamide was detected in the extract of A. craccivora that infested R. pseudoacacia (7.7 μg/g fresh weight) but not in that infesting V. angustifolia. The toxicity of canavanine, 2-aminoethanol, and cyanamide was evaluated against H. axyridis larvae in a bioassay by using an artificial diet containing these compounds at various concentrations. Cyanamide exhibited 10-100 times stronger toxicity than canavanine and 2-aminoethanol. These results indicate that the toxicity is at least partly due to cyanamide, which is present in the toxic A. craccivora that infests R. pseudoacacia but absent from the non-toxic A. craccivora that infests V. angustifolia.

Concepts: Insect, Toxicity, Fabaceae, Vicia, Aphid, Coccinellidae, Harmonia axyridis, Robinia pseudoacacia

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BACKGROUND: The harlequin ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae) is native to central and eastern Asia and was purposely introduced into Europe to control aphids. While it proved to be a good biological control agent, its rapid spread and buildup of large populations made it a nuisance, since it overwinters in homes, emits unpleasant odors, stains fabrics, occasionally bites humans and feeds on apples, pears and grapes. Aside from the above, the ravenous appetite of H. axyridis results in their consumption of harmless native insects, including even other ladybird beetles. A study of the natural enemies of H. axyridis in Denmark revealed the presence of nematodes. The present study describes this nematode parasite and discusses aspects of its development and ecology. METHODS: Adult harlequin ladybird beetles were collected from March to November from four localities in Copenhagen on different plant species. In addition, groups of last-instar larvae and pupae (n = 50) were examined for the presence of nematodes. Living and recently dead nematodes were removed from adult H. axyridis in 0.5% saline solution, the nematodes were then heat killed (at 75 C), fixed in 5% formalin and transferred to glycerin on slides for further examination and measurements. RESULTS: A new species of Allantonematidae (Tylenchida), Parasitylenchus bifurcatus n. sp., is described from adults of the harlequin ladybird, Harmonia axyridis in Denmark. The new species is characterized by a straight stylet lacking basal thickenings, a bursa and a forked tail tip in the vermiform (infective) females and juvenile males. The new species is compared with P. coccinellinae previously described from ladybird beetles in France. Parasitism resulted in depletion of the fat body and partial or complete atrophy of the reproductive organs of the beetles. Infections occurred throughout the year with rates of parasitism reaching up to 35%. The rate increased to 60% when field-collected ladybirds were incubated for 30 days in the laboratory. CONCLUSIONS: The production of subsequent generations within the host with only the fertilized females (not the males) leaving the hosts and the absence of parasitism of the larvae and pupae is an impressive developmental modification of P. bifurcatus. It is proposed that the vermiform (infective) females pass from one adult host to another when the beetles are hibernating or in assemblage groups. Rates of parasitism show that P. bifurcatus could be a significant biological control agent of H. axyridis.

Concepts: Insect, Nematode, Beetle, Parasitoid, Beetles, Aphid, Coccinellidae, Harmonia axyridis

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Understanding the characteristics and drivers of dispersal is crucial for predicting population dynamics, particularly in range-shifting species. Studying long-distance dispersal in insects is challenging, but recent advances in entomological radar offer unique insights. We analysed 10 years of radar data collected at Rothamsted Research, U.K., to investigate characteristics (altitude, speed, seasonal and annual trends) and drivers (aphid abundance, air temperature, wind speed and rainfall) of high-altitude flight of the two most abundant U.K. ladybird species (native Coccinella septempunctata and invasive Harmonia axyridis). These species cannot be distinguished in the radar data since their reflectivity signals overlap, and they were therefore analysed together. However, their signals do not overlap with other, abundant insects so we are confident they constitute the overwhelming majority of the analysed data. The target species were detected up to ∼1100 m above ground level, where displacement speeds of up to ∼60 km/h were recorded, however most ladybirds were found between ∼150 and 500 m, and had a mean displacement of 30 km/h. Average flight time was estimated, using tethered flight experiments, to be 36.5 minutes, but flights of up to two hours were observed. Ladybirds are therefore potentially able to travel 18 km in a “typical” high-altitude flight, but up to 120 km if flying at higher altitudes, indicating a high capacity for long-distance dispersal. There were strong seasonal trends in ladybird abundance, with peaks corresponding to the highest temperatures of mid-summer, and warm air temperature was the key driver of ladybird flight. Climatic warming may therefore increase the potential for long-distance dispersal in these species. Low aphid abundance was a second significant factor, highlighting the important role of aphid population dynamics in ladybird dispersal. This research illustrates the utility of radar for studying high-altitude insect flight and has important implications for predicting long-distance dispersal.

Concepts: Insect, Temperature, Aphid, Coccinellidae, Harmonia axyridis, Coccinella septempunctata, Biological pest control agents, Coccinella

2

The use of biological control agents to control pests is an alternative to pesticides and a tool to manage invasive alien species. However, biocontrol agents can themselves become invasive species under certain conditions. The harlequin ladybird (Harmonia axyridis) is a native Asian biocontrol agent that has become a successful invader. We reviewed articles containing “Harmonia axyridis” to gather information on its presence and surveyed entomologists researching Coccinellidae around the world to investigate further insights about the current distribution, vectors of introduction, habitat use and threats this species pose. The harlequin ladybird has established populations in at least 59 countries outside its native range. Twenty six percent of the surveyed scientists considered it a potential threat to native Coccinellidae. Published studies and scientists suggest Adalia bipunctata, native to Europe, is under the highest risk of population declines. Strict policies should be incorporated to prevent its arrival to non-invaded areas and to prevent further expansion range. Managing invasive species is a key priority to prevent biodiversity loss and promote ecosystem services.

Concepts: Biodiversity, Biology, Ecology, Biological pest control, Invasive species, Coccinellidae, Harmonia axyridis, Biological pest control agents

2

Hesperomyces virescens is a fungal ectoparasite (Laboulbeniales) that infects adult ladybirds. Research has recently focused on this parasite due to the discovery of its prevalence on the globally invasive harlequin ladybird Harmonia axyridis and for its potential use in studies of co-evolution and pathogen spread. We collected adults from ten species of ladybirds in the Western Cape Province, South Africa, and screened for the presence of H. virescens. Infections with H. virescens were found in the samples of two species, H. axyridis and the native Cheilomenes propinqua. This marks the first record of H. virescens on H. axyridis from the African continent and the first record on Cheilomenes worldwide.

Concepts: Bacteria, Africa, Fungus, South Africa, Beetle, Western Cape, Coccinellidae, Harmonia axyridis