Substrate Marking by an Invasive Ladybeetle: Seasonal Changes in Hydrocarbon Composition and Behavioral Responses

Abstract

The multicolored Asian ladybeetle, Harmonia axyridis (Pallas), aggregates inside dwellings during the winter to survive the cold. Recent published reports have highlighted that overwintering individuals use hydrocarbon markings deposited on surfaces by conspecifics to orient toward aggregation sites. In the current study, monthly GC-MS analyses revealed seasonal modifications in the chemical profile of substrate markings deposited by moving individuals. The markings of overwintering ladybeetles contained larger proportions of heptacosadiene, nonacosadiene, hentriacontadienes, and methyl-nonacosanes, along with a lower proportion of heptacosene and nonacosene. This finding suggests the importance of the unsaturated and/or branched hydrocarbons in the H. axyridis aggregation process. Subsequently, we conducted behavioral assays to test whether (1) there is seasonal variation in the behavioral response of H. axyridis individuals toward substrate markings deposited by conspecifics in the same physiological state and (2) the observed behavioral modification is due to a change in ladybeetle sensitivity and/or a change in the chemical composition of the substrate marking. The results indicate that overwintering individuals exhibit a stronger “following” response toward conspecific substrate markings. This behavior is linked to both the physiological state of ladybeetles and the specific chemical profile of the marking biomolecules deposited under overwintering conditions.

Behavioral and Immunological Features Promoting the Invasive Performance of the Harlequin Ladybird Harmonia axyridis

“…Non-volatile long-chain hydrocarbons are passively deposited by walking males and females on the surfaces surrounding the aggregation site (Kosaki and Yamaoka, 1996;Durieux et al, 2012). The chemical composition of the marking varies with the season, being richer in unsaturated hydrocarbons in winter than in summer (Durieux et al, 2013). Overwintering individuals are also more likely to follow this chemical mark than individuals collected in spring or summer.…”

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

“…Evidence is accumulating regarding the important roles that hydrocarbons play in lady beetles (Fassotte et al, 2016). Hydrocarbons are found in larval tracks, adult footprints and elytra, and are also involved in the location of overwintering sites or the detection of competitors (Hemptinne et al, 1998;Nakashima et al, 2006;Magro et al, 2010;Durieux et al, 2012Durieux et al, ,2013Susset et al, 2013;Wheeler & Cardé, 2014;Verheggen et al, 2017). Furthermore, there is no doubt that elytra hydrocarbons are involved in mate selection.…”

Evolutionary ecology of microsporidia associated with the invasive ladybird Harmonia axyridis

“…Chemical defense Harmonine-mediated protection against parasites and pathogens Röhrich et al (2012) Harmonine-mediated protectionof eggs against intraguild predation Kajita et al (2010) Immunity High resistance against entomopatogenic fungi which is conferred by a diverse spectrum of antimicrobial peptides Vilcinskas et al (2013a) Parasites Tolerance against microsporidia which can infect native ladybird species Vilcinskas et al (2013b) Spiroplasma-infection increases body size and fecundity Elnagdy et al (2013) Reproduction Invasive males have higher reproductive success, and invasive females reproduce sooner and yield more eggs, which are fertilized by larger number of fathers Laugier et al (2013) Population genetics Absence of inbreeding depression in introduced populations results in a population bottleneck of intermediate size that purges deleterious mutations in the first stages of the invasion process Facon et al (2011) Stress adaptation Adaptation to a broad temperature range, thus allowing long migrations to over-wintering sites Majerus et al (2006) Behavior Increased flight speed promotes dispersal in invasive populations Lombaert et al (2014) Aggregation of invasive populations at overwintering sites Durieux et al (2013) Success in intraguild predation with native competitors Gardiner et al (2011)…”

“…H. axyridis is also well adapted to a broad temperature range, thus allowing long migrations to overwintering sites (Majerus et al, 2006). The aggregation behavior at overwintering sites may also reflect adaptation of invasive populations to areas with cold winters (Durieux et al, 2013).…”