Harmonia axyridis: how to explain its invasion success in Europe

Abstract of the thesis entitled “Harmonia axyridis: how to explain its invasion success in Europe” After introduction as biological control agent of aphids, the multicoloured Asian ladybird Harmonia axyridis has established and spread in Europe. Harmonia axyridis is now regarded as an invasive species because its establishment had negative effects on non-target species, fruit production, and human health. Life history characteristics were studied in order to find an explanation for its invasion success. With a meta-analysis I showed that life-history traits of H. axyridis differed between Asian and invasive populations of H. axyridis. However, the greatest differences in development rate were observed at temperatures above 24°C, while at temperatures characteristic for spring and summer in northwestern Europe (17 to 24°C) invasive populations of H. axyridis do not differ from native Asian populations; thus, the invasive success cannot be attributed to a change in life history characteristics of the invasive population. Compared to native species European ladybirds (Adalia bipunctata, Coccinella septempunctata, and Propylea quatuordecimpunctata), H. axyridis develops slower and starts reproduction later, suggesting no competitive advantage for the invader. Additionally, life history characteristics were studied under field conditions. I showed that in northwestern Europe H. axyridis has a period of real diapause starting at the end of October and shifts to a quiescent state in December. This diapause is relatively short and weak compared with published data of native ladybirds. Moreover, it appears to have become shorter over the last decade. Thus, H. axyridis can become active rapidly when temperature rises in spring, but, nevertheless, it is not reported to be active earlier in the year than native species. Overwintering survival of H. axyridis in the Netherlands is between 71 and 88%. At five sample sites I found that ladybirds that were hibernating at the southwestern sides of buildings, where most aggregations of ladybirds were found, had a higher winter survival than ladybirds hibernating at other orientations. At sheltered sites survival was higher compared to exposed sites. A high overwintering survival results in a large post-hibernation population and a rapid population build-up in spring. Compared with most common native species, winter survival of H. axyridis is similar or higher. In this research, i.e. under semi-field conditions, immature survival of H. axyridis and A. bipunctata reached high levels, but survival was generally considerably higher for H. axyridis than for the native A. bipunctata. Under semi-field conditions with high food availability, no effect of the presence of H. axyridis on the survival, development, weight, and size of the native species A. bipunctata was found. Under natural conditions, however, situations of prey scarcity do occur, as aphid colonies are relatively short-lived. Additionally, I demonstrated that in absence of food under semi-field conditions, intraguild predation between C. septempunctata, A. bipunctata, and H. axyridis does occur, although the contact frequency is low. When two fourth instar larvae were placed together on a single leaf, at least one contact was made in 23–43% of the observations, depending on the tested species combination. When contacts between ladybirds do occur, H. axyridis larvae are the winners in contacts with larvae of the native species. Finally, I found that several natural enemies are starting to use H. axyridis as a host but are as yet not sufficiently abundant and/or effective to have a profound impact on populations of the invader. In the years 2003—2007 no natural enemies were found in ladybird samples. From 2008 onwards H. axyridis adults were infested by: Hesperomyces virescens fungi (summer and winter), Parasitylenchus bifurcatus nematodes (winter), Coccipolipus hippodamiae mites (winter), and Dinocampus coccinellae parasitoids (summer and winter). Summarising, the successful invasion of H. axyridis in the Netherlands cannot be explained by a change of the invasive H. axyridis populations in comparison with the native Asian population, but by a combination of several characteristics: overwintering, immature survival, fecundity, longevity, number of generations per year, and intraguild predation. In comparison with native European ladybird species, H. axyridis survives better (in winter and the immature stages), it lays more eggs, has more generations per year, and lives longer: this results in a faster population growth than that of native ladybirds. Harmonia axyridis can potentially easily outnumber native species within a few years. Moreover, H. axyridis being a strong intraguild predator, the slow immature development and late arrival at aphid colonies compared to native species is compensated by the ability of H. axyridis to feed on eggs, larvae, and pupae of other ladybirds, thereby completing its development. However, several facts, e.g. the quite stable diversity and abundance of ladybird species in Asia and the first evidence that natural enemies attack H. axyridis, suggest that the current situation in Europe may not be the terminal stage, but a transition to a new balance where native species are strongly reduced in abundance, but do not become extinct.

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Bibliographic Details
Main Author: Raak-van den Berg, C.L.
Other Authors: van Lenteren, Joop
Format: Doctoral thesis biblioteca
Language:English
Published: Wageningen University
Subjects:biological control agents, feeding behaviour, harmonia axyridis, introduced species, invasive alien species, netherlands, predation, geïntroduceerde soorten, invasieve exoten, nederland, organismen ingezet bij biologische bestrijding, predatie, voedingsgedrag,
Online Access:https://research.wur.nl/en/publications/harmonia-axyridis-how-to-explain-its-invasion-success-in-europe
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Summary:Abstract of the thesis entitled “Harmonia axyridis: how to explain its invasion success in Europe” After introduction as biological control agent of aphids, the multicoloured Asian ladybird Harmonia axyridis has established and spread in Europe. Harmonia axyridis is now regarded as an invasive species because its establishment had negative effects on non-target species, fruit production, and human health. Life history characteristics were studied in order to find an explanation for its invasion success. With a meta-analysis I showed that life-history traits of H. axyridis differed between Asian and invasive populations of H. axyridis. However, the greatest differences in development rate were observed at temperatures above 24°C, while at temperatures characteristic for spring and summer in northwestern Europe (17 to 24°C) invasive populations of H. axyridis do not differ from native Asian populations; thus, the invasive success cannot be attributed to a change in life history characteristics of the invasive population. Compared to native species European ladybirds (Adalia bipunctata, Coccinella septempunctata, and Propylea quatuordecimpunctata), H. axyridis develops slower and starts reproduction later, suggesting no competitive advantage for the invader. Additionally, life history characteristics were studied under field conditions. I showed that in northwestern Europe H. axyridis has a period of real diapause starting at the end of October and shifts to a quiescent state in December. This diapause is relatively short and weak compared with published data of native ladybirds. Moreover, it appears to have become shorter over the last decade. Thus, H. axyridis can become active rapidly when temperature rises in spring, but, nevertheless, it is not reported to be active earlier in the year than native species. Overwintering survival of H. axyridis in the Netherlands is between 71 and 88%. At five sample sites I found that ladybirds that were hibernating at the southwestern sides of buildings, where most aggregations of ladybirds were found, had a higher winter survival than ladybirds hibernating at other orientations. At sheltered sites survival was higher compared to exposed sites. A high overwintering survival results in a large post-hibernation population and a rapid population build-up in spring. Compared with most common native species, winter survival of H. axyridis is similar or higher. In this research, i.e. under semi-field conditions, immature survival of H. axyridis and A. bipunctata reached high levels, but survival was generally considerably higher for H. axyridis than for the native A. bipunctata. Under semi-field conditions with high food availability, no effect of the presence of H. axyridis on the survival, development, weight, and size of the native species A. bipunctata was found. Under natural conditions, however, situations of prey scarcity do occur, as aphid colonies are relatively short-lived. Additionally, I demonstrated that in absence of food under semi-field conditions, intraguild predation between C. septempunctata, A. bipunctata, and H. axyridis does occur, although the contact frequency is low. When two fourth instar larvae were placed together on a single leaf, at least one contact was made in 23–43% of the observations, depending on the tested species combination. When contacts between ladybirds do occur, H. axyridis larvae are the winners in contacts with larvae of the native species. Finally, I found that several natural enemies are starting to use H. axyridis as a host but are as yet not sufficiently abundant and/or effective to have a profound impact on populations of the invader. In the years 2003—2007 no natural enemies were found in ladybird samples. From 2008 onwards H. axyridis adults were infested by: Hesperomyces virescens fungi (summer and winter), Parasitylenchus bifurcatus nematodes (winter), Coccipolipus hippodamiae mites (winter), and Dinocampus coccinellae parasitoids (summer and winter). Summarising, the successful invasion of H. axyridis in the Netherlands cannot be explained by a change of the invasive H. axyridis populations in comparison with the native Asian population, but by a combination of several characteristics: overwintering, immature survival, fecundity, longevity, number of generations per year, and intraguild predation. In comparison with native European ladybird species, H. axyridis survives better (in winter and the immature stages), it lays more eggs, has more generations per year, and lives longer: this results in a faster population growth than that of native ladybirds. Harmonia axyridis can potentially easily outnumber native species within a few years. Moreover, H. axyridis being a strong intraguild predator, the slow immature development and late arrival at aphid colonies compared to native species is compensated by the ability of H. axyridis to feed on eggs, larvae, and pupae of other ladybirds, thereby completing its development. However, several facts, e.g. the quite stable diversity and abundance of ladybird species in Asia and the first evidence that natural enemies attack H. axyridis, suggest that the current situation in Europe may not be the terminal stage, but a transition to a new balance where native species are strongly reduced in abundance, but do not become extinct.