Interspecific Interactions between the Invasive Beetle Harmonia axyridis, Native Anthocorids and Entomopathogenic Fungi

Andrew Gordon Howe

Abstract

The Earth’s biodiversity encompasses dynamic arrangements of ecosystems, species and their inherent genetic diversity. Biodiversity is an integral component underlying functional ecosystems. Human well-being is dependent on a variety of services provided by ecosystems, e.g. climate regulation, pest suppression and provision of clean water. Concurrently, direct and indirect human influences can impinge biodiversity thereby disrupting ecosystem services. Understanding humanmediated drivers of biodiversity change will enhance sustainable use of ecosystems now and in the future. Increased global trade, travel and tourism are linked to biodiversity change. These drivers can inadvertently increase biotic exchange of species between regions, countries and continents, while deliberate species introductions have the same effect, e.g. release of biological control agents. Biotic exchange is considered negative when introduced species cause negative impacts on ecosystems, or cause economic or human detriment, i.e. biological invasions. Rates of biological invasion are more intense now than previously detected in prehistoric records and are recognized as a major threat to global biodiversity. The harlequin ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) was introduced to North America from Asia in the early 20th century as a biological control agent against insect agricultural pests. In the late 20th century a specific population in eastern North America became invasive. Invasive H. axyridis have since spread to many countries on 4 continents. Evidence shows native predatory insect species are negatively impinged. There is concern that decline of native predatory insects may alter the regulating ecosystem service provided by these natural enemies, i.e. pest suppression. Most of our knowledge of H. axyridis impacts on biodiversity stem from studies on ladybirds associated with agricultural habitat. Furthermore, studies largely focus on intraguild predation, a direct trophic interaction whereby H. axyridis attacks a native species with which it competes with for a resource, e.g. aphids. However, a vast assemblage of predators other than ladybirds may be affected by invasive H. axyridis, while other interspecific interactions may also be implicated. This PhD thesis addresses an indirect trophic interaction, namely interspecific competition, between H. axyridis and Anthocoris nemoralis (Heteroptera: Anthocoridae), a European flower bug which shares habitat and prey with invasive H. axyridis in urban habitats. Interspecific competition occurs when species compete for limited resources, and can reduce predator fitness and contribute to species displacement. This was approached through laboratory assays which assessed the relative strength of interspecific competition compared to intraguild predation and possible effects thereof on predators. A field-based study using DNA gut-content analysis tested whether trophic interactions between co-occurring predators in urban arboreal habitats reflected findings from laboratory assays. In addition, infection of H. axyridis by naturally occurring entomopathogenic fungi was assessed in order to determine whether fungi co-occur with ladybirds in arboreal habitats and whether entomopathogenic fungi exploit H. axyridis. Finally, in an attempt to shed light on the role of insect behaviour in biological invasions, a supplementary dataset compared behavioural 8 traits (tendency to fly/mate and activity) relevant to successful invasion between five native/invasive H. axyridis populations. Findings from laboratory assays strongly suggested interspecific competition with H. axyridis is a stronger interaction for A. nemoralis than intraguild predation by H. axyridis. This was manifest through reduced survival and a sublethal effect on A. nemoralis fitness (weight gain). In urban arboreal habitats, DNA gut-content analysis revealed a low level of intraguild predation by H. axyridis, but a high level of prey overlap between predators, thereby confirming the relative strengths of interspecific interactions among wild populations. Coupled with high temporal and spatial niche overlap of predators these findings demonstrate that interspecific competition for resources by H. axyridis has the potential to affect local populations of native predatory insects whose habitat is invaded by H. axyridis. Five species of naturally occurring entomopathogenic fungi from three genera were distributed in arboreal habitats, however two of these genera were responsible for most fungi prevalence in H. axyridis and native ladybirds. These novel findings demonstrate that trees are a source of infection, which suggests that entomopathogenic fungi contribute to regulation of H. axyridis populations in invaded urban habitats. Finally, comparison of behaviours revealed that an invasive eastern North American and native Chinese population displayed greater dispersal activity than three other populations. Although an invasive/native dichotomy was not established, results suggest that trait differences may reflect population-level adaptions. Findings underline that intraspecific comparisons of an invasive species’ native and introduced populations may uncover traits which play a role in biological invasions. This PhD thesis contributes novel insights into interspecific interactions involving the harlequin ladybird which have implications for species coexistence in invaded ecosystems. Concurrently, the strength of trophic interactions between ladybirds and fungi were assessed in urban ecosystems, which addresses the paucity of knowledge in ecosystems beyond agricultural habitats while also contributing to basic ecological knowledge of fungi. Findings highlight the importance of assessing indirect interspecific trophic interactions as they potentially affect a wider range of taxa than direct interspecific interactions, e.g. intraguild predation.

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