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Title: The role of parasites in the invasion ecology of Harmonia axyridis
Author: Berry, Katharine M.
ISNI:       0000 0004 7226 9025
Awarding Body: University of Stirling
Current Institution: University of Stirling
Date of Award: 2017
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The success of an invasive alien species is often attributed to the ecological advantage gained from natural enemy release. Numerous factors have been suggested as contributing to the success of Harmonia axyridis as an invasive alien species, including enemy release. This thesis studied the interactions of several parasites with H. axyridis, investigating parasite transmission, growth and virulence as well as host immune responses, thereby shedding light on the potential role of enemy release in the invasion biology of this ladybird. Benefits gained by invasive alien species from enemy release diminish if parasites of native species shift hosts to exploit the novel invader. The fungal ectoparasite Hesperomyces virescens began infecting H. axyridis shortly after it invaded the UK, probably as a result of a host shift from Adalia bipunctata. This study found a rapid increase in H. virescens prevalence over three years in London H. axyridis populations. Laboratory study showed H. virescens transmission and growth to be more efficient on A. bipunctata than the novel host. In addition, reciprocal interspecific transfers of H. virescens strains isolated from A. bipunctata and H. axyridis revealed that the infection characteristics of the fungi from these two hosts differed, suggesting strains may have diverged after the initial shift from A. bipunctata to better exploit the host from which they were derived. Laboulbenialian fungi were previously thought to have negligible impacts on host fitness. A detailed examination of H. virescens infecting H. axyridis found distinct virulence, with infections resulting in a 50% reduction in host lifespan. In addition, chronic H. virescens infection in males caused acceleration in the age-associated decline in body condition while for females, infection triggered fecundity senescence and a faster age-related decline in fertility. While their role in accelerating ageing is debated, the results presented here provide evidence that infectious diseases can drive the ageing process in this insect species. In nature, multiple parasites affecting a single host are common. The effect of co-infection on the virulence caused by two fungal infections was characterised using H. axyridis and A. bipunctata hosts. The ability of two ladybird species to defend against an acute fungal parasite, while infected with the relatively avirulent H. virescens was found to be sex-specific. While for females, the presence of co-infection did not alter the virulence seen in singly infected females, a higher mortality rate existed for co-infected males compared with those infected singly. Previously, H. virescens has been considered to be avirulent, however, this study provides evidence that this chronic fungal parasite may be important when considering the mortality associated with co-infections in the field. The invasive success of H. axyridis has, in part, been attributed to a more vigorous immune ability compared with other competitor species. Previously, field studies have shown that the prevalence of the parasitoid wasp Dinocampus coccinellae in H. axyridis is considerably lower than in the UK primary host of this wasp, Coccinella septempunctata. The extent to which the prevalence asymmetry in the field is driven by differences in host encapsulation response was tested by first comparing the encapsulation ability of C. septempunctata and H. axyridis directed against an artificial implant. Following this, the encapsulation response of D. coccinellae parasitized individuals was assessed and compared between the two host species. While encapsulation ability did not differ between the host species, and D. coccinellae did not affect the immune response of H. axyridis, wasp parasitism did alter the encapsulation ability of C. septempunctata, although it was inconsistent across sexes and populations. Overall, this thesis furthers our understanding of the fungal parasite H. virescens and its association with the notorious invader H. axyridis. The research presented here also demonstrates the use of H. axyridis as a model system in areas other than invasion ecology and furthermore, contributes to understanding the role of infectious disease in the rate of ageing. Finally, sex-specific effects were found across the chapters of this thesis, demonstrating the use of H. axyridis in the study of sex-specific effects of infections.
Supervisor: Tinsley, Matthew ; Roy, Helen ; Bussiere, Luc Sponsor: NERC
Qualification Name: Thesis (Ph.D.) Qualification Level: Doctoral
EThOS ID:  DOI: Not available
Keywords: ladybird ; invasion ecology ; parasite ; harmonia axyridis ; Ladybugs ; Host-parasite relationships ; Biological invasions