Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas

Authors: CERYNGIER, PIOTR - Cardinal Stefan Wyszynski University In Warsaw; NEDVED, OLDRICH - University Of South Bohemia; GREZ, AUDREY - Universidad De Chile; Riddick, Eric; ROY, HELEN - Centre For Ecology And Hydrology; SAN MARTIN, GILLES - Walloon Agricultural Research Center; STEENBERG, TOVE - Aarhus University; VESELY, PETR - University Of South Bohemia; ZAVIEZO, TANIA - Pontifical Catholic University Of Chile; ZUNIGA-REINOSO, ALVARO - Universidad De Chile; HAELEWATERS, DANNY - Harvard University

Submitted to: Biological Invasions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/25/2017
Publication Date: 4/25/2018
Citation: Ceryngier, P., Nedved, O., Grez, A.A., Riddick, E.W., Roy, H.E., San Martin, G., Steenberg, T., Vesely, P., Zaviezo, T., Zuniga-Reinoso, A., Haelewaters, D. 2018. Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas. Biological Invasions. 20(4):1009-1031.

Interpretive Summary: Despite the evidence of its effectiveness as a natural enemy of pest insects on crop plants in agroecosystems in North America, the harlequin ladybird beetle (i. e., multicolored Asian lady beetle) is currently regarded as an invasive species, because of its ability to out-compete other ladybird species in invaded countries. The rapid expansion of the harlequin into other countries has not abated, even after nearly two decades of documented migration. One possible reason for the successful invasion of the harlequin is that its repertoire of natural enemies (naturally-occurring predators and parasitoids) are lacking or not abundant in the invaded countries. This paper compiles and synthesizes the available literature on predators and parasitoids of the harlequin on a global scale. The results indicate that vertebrate and invertebrate predators in invaded countries are rather ineffective, thus incapable of reducing range expansion of this ladybird. Invertebrate parasitoids have limited effect on harlequin populations, but several true fly species (in the family Phoridae) might have the capacity to circumvent physiological and immunological defenses of the harlequin and exert some control over its populations in the near future.

Technical Abstract: The harlequin ladybird Harmonia (H.) axyridis (Coleoptera:Coccinellidae) has rapidly spread in several continents over the past 30 years and is considered an invasive alien species. The success of H. axyridis as an invader is often attributed to weak control by natural enemies. In this paper, we provide an overview of current knowledge on predators and parasitoids of H. axyridis. The common feature of predators and parasitoids is that they directly kill exploited organisms. Currently available data show that H. axyridis, displaying a variety of chemical, mechanical, and microbiological antipredator defenses, is usually avoided by predators. However, some birds and invertebrates can eat this ladybird without harmful consequences. The primary defenses of H. axyridis against parasitoids include immune response and physiological and nutritional unsuitability for parasitoid development. These defenses are probably relatively efficient against most ladybird parasitoids, but not against flies of the genus Phalacrotophora. The latter are idiobiont parasitoids and hence can evade the host's immune response. Indeed, rates of parasitism of H. axyridis by Phalacrotophora in the Palaearctic region (both in the native range in Asia and in Europe) are relatively high. While strong evidence for enemy release on the invasive populations of H. axyridis is lacking, several cases of parasitoid acquisition have been recorded in Europe, North America, and South America. We conclude that enemy release cannot be excluded as a possible mechanism contributing to the spread and increase of H. axyridis in the early stages of invasion, but adaptation of parasitoids may lead to novel associations which might offset previous effects of enemy release. However, further work is required to elucidate the population-level effects of such interactions.