- Proceedings. Biological sciences / The Royal Society
- Published over 7 years ago
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.
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.
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.
A rape seed pollen-based diet was developed and found to be suitable for use in a dietary exposure assay for Propylea japonica. Using the diet, we established and validated a dietary exposure assay by using the protease inhibitor E-64 as positive control. Dose-dependent responses were documented for all observed life-table parameters of P. japonica including survival, pupation and eclosion rates, development time and adult weight. Results suggested that the dietary assay can detect the effects of insecticidal compounds on the survival and development of P. japonica. Using the established dietary assay, we subsequently tested the toxicity of Cry1Ab, Cry1Ac and Cry1F proteins that are expressed by transgenic maize, cotton or rice plants to P. japonica larvae. The diet containing E-64 was included as a positive control. Survival and development of P. japonica larvae were not adversely affected when the diet contained purified Cry1Ab, Cry1Ac, or Cry1F at 500 µg/g diet representing a worst-case exposure scenario. In contrast, P. japonica larvae were adversely affected when the diet contained E-64. The bioactivity and stability of the Cry proteins in the diet and Cry protein uptake by the ladybird larvae were confirmed by bioassay with a Cry-sensitive insect species and by ELISA. The current study describes a suitable experimental system for assessing the potential effects of gut-active insecticidal compounds on ladybird beetle larvae. The experiments with the Cry proteins demonstrate that P. japonica larvae are not sensitive to Cry1Ab, Cry1Ac and Cry1F.
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.
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.
The recent development of very high resistance to phosphine in rusty grain beetle, Cryptolestes ferrugineus (Stephens), seriously threatens stored-grain biosecurity. The aim was to characterise this resistance, to develop a rapid bioassay for its diagnosis to support pest management and to document the distribution of resistance in Australia in 2007-2011.
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.
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.
Abstract Ladybird beetles are generally considered as agriculturally beneficial insects, but the ladybird beetles in the coleopteran subfamily Epilachninae are phytophagous and major plant feeding pest species which causes severe economic losses to cucurbitaceous and solanaceous crops. Henosepilachna pusillanima (Mulsant) is one of the important pest species of ladybird beetle. In this report, we sequenced and characterized the complete mitochondrial genome of H. pusillanima. For sequencing of the complete mitochondrial genome, we used the Ion Torrent sequencing platform. The complete circular mitochondrial genome of the H. pusillanima was determined to be 16,216 bp long. There were totally 13 protein coding genes, 22 transfer RNA, 2 ribosomal RNA and a control (A + T-rich) region estimated to be 1690 bp. The gene arrangement and orientations of assembled mitogenome were identical to the reported predatory ladybird beetle Coccinella septempunctata L. This is the first completely sequenced coleopteran mitochondrial genome from the beetle subfamily Epilachninae from India. Data generated in this study will benefit future comparative genomics studies for understanding the evolutionary relationships between predatory and phytophagous coccinellid beetles.