A Well Protected Intruder: The Effective Antimicrobial Defense of the Invasive Ladybird Harmonia axyridis

Abstract

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) is a polyphagous predatory beetle native to Central and Eastern Asia. Since 2007 it has established all over Central Europe. In order to elucidate which defense strategy is responsible for its high resistance to diseases, we tested hemolymph as well as eleven main components of the headspace of H. axyridis for antimicrobial activity against Gram-positive (Bacillus subtilis, B. thuringiensis ssp. tenebrionis, Micrococcus luteus) and Gram-negative bacteria (Escherichia coli) and yeast (Saccharomyces cerevisiae). While three of the volatile compounds weakly reduced the growth of microorganisms, hemolymph of adults and larvae of H. axyridis strongly inhibited the growth of Gram-positive and Gram-negative bacteria as well as yeast. Furthermore, we compared the antimicrobial activity in the hemolymph of H. axyridis and Coccinella septempunctata. Antimicrobial activity in H. axyridis was about a thousand times higher compared to hemolymph from C. septempunctata. In contrast to C. septempunctata, the antimicrobial activity in H. axyridis was present without prior challenge. Minimal inhibitory concentration (MIC) of the hemolymph of H. axyridis was lowest against E. coli and yeast followed by B. subtilis, and was highest against entomopathogenic B. thuringiensis ssp. tenebrionidae. Furthermore, MIC values of the hemolymph obtained from live beetles were significantly lower than from frozen insects. This suggests that the active antimicrobial compound is affected by freezing and subsequent thawing of the beetles. Potential implications of our findings for the competitive advantages of H. axyridis over C. septempunctata are discussed.

Puncture vs. reflex bleeding: Haemolymph composition reveals significant differences among ladybird species (Coleoptera: Coccinellidae), but not between sampling methods

“…This method is rarely used (Gross et al, 2010) and there is no corresponding methodological study. The use of refl ex blood as a source of haemolymph could be benefi cial, especially in studies where repeated sampling from adult ladybirds is needed and injury caused by puncturing would have an undesired effect on the response of the insect studied.…”

“…A very effi cient immune system is thought to be responsible for the worldwide invasive success of Harmonia axyridis (Vogel et al, 2017). However, comparisons are limited to only a few other species of ladybirds -Coccinella septempunctata and Adalia bipunctata (Gross et al, 2010;Schmidtberg et al, 2013;Vogel et al, 2017). Here we show that another ladybird species native to Europe, namely Ceratomegilla undecimnotata, has a humoral antimicrobial defence against Escherichia coli comparable to that of the invasive species, Harmonia axyridis.…”

Multifaceted Defense against Antagonistic Microbes in Developing Offspring of the Parasitoid Wasp Ampulex compressa (Hymenoptera, Ampulicidae)

“…There are, however, some studies dealing with the possible role of volatile organic compounds as antimicrobials in insects [6], [7], [24], [67], [68], [69], [70], [71], [72], [73]. The volatiles naphthalene and fenchone that are present in the nest of Coptotermes formosanus termites have been hypothesized to act as fumigants in the closed nest to inhibit microorganisms [67], [68], [69], [70].…”

“…Owing to the persistent selection pressure exerted by detrimental microorganisms, insects have evolved diverse sophisticated antimicrobial strategies to defend themselves, their offspring, and their foods from microbial pathogens and decomposers [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], [13]. The remedial measures include complex immune systems [14], [15], behavioral adaptations [16], [17], [18], defensive symbiosis [9], [19], [20], [21], and the deployment of chemical compounds with antimicrobial effects [1], [2], [7], [22], [23], [24].…”

Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids?

“…However, the invasive alien harlequin ladybird, H. axyridis, is more resistant than closely related native coccinellids to a number of natural enemies, including the generalist entomopathogenic fungus Beauveria bassiana Balsamo (Hypocreales: Cordycipitaceae) (Roy et al 2008), entomopathogenic nematodes (Shapiro-Ilan and Cottrell 2005), Dinocampus coccinellae (Schrank) (Hymenoptera: Braconidae) (Koyama and Majerus 2008;Berkvens et al 2010) and microbes (Gross et al 2010). Interestingly, Roy et al (2008) demonstrated that the invasive alien population of H. axyridis in Britain was more resistant to B. bassiana than a population from native Japan, so supporting the EICA.…”