Ecology and evolution of Cardiaspina psyllids, their bacterial endosymbionts and parasitoid wasps

Identifying, classifying and ranking the major factors and processes influencing population dynamics and community structure of animals are the greatest challenges of ecological research. Examples of these factors and processes are climate, competition, resource limitation, natural enemies and symbionts. Cardiaspina (Hemiptera: Aphalaridae) are psyllids that specifically feed on Eucalyptus and are well known for experiencing major population outbreaks that can result in area-wide defoliation. An outbreak of a Cardiaspina sp. of uncertain species assignment on Eucalyptus moluccana (Grey Box) in the critically endangered Cumberland Plain Woodland of Western Sydney that had started just prior to the start of this PhD project provided an ideal case study to investigate the factors and processes driving this major herbivore outbreak during its peak and decline (Chapter 2). Minimum winter temperature differences in different study sites of the fragmented woodland across the large outbreak region had a significant direct impact on psyllid population development and distribution. Furthermore, winter temperature may have indirectly impacted outbreak dynamics via constrained parasitoid aggregation between study sites due to host developmental differences. Resource depletion due to area-wide defoliation and summer heat waves were responsible for the dramatic decline in psyllid populations that occurred during this study, while the principal natural enemies (parasitoid wasps) did not appear to play a significant role. Parasitoid wasps were inhibited in their regulation of the psyllid outbreak by a greater mortality rate in larval stages than their psyllid host. Parasitised hosts were more susceptible than unparasitised hosts to mortality brought about by host overabundance (resulting into intraspecific psyllid competition), and summer heat waves. Larval parasitoid mortality, loss of life cycle synchrony between woodland fragments and hyperparasitisation of parasitoids by hyperparasitoids all appeared to contribute to parasitisation being inversely density dependent to host density. It was concluded that this may provide a general explanation for the low incidence of reported density dependence of parasitisation in natural ecosystems, in particular during outbreaks, and therefore when host density is high. At a different trophic level, psyllids harbour bacterial endosymbionts. Carsonella (Gammaproteobacteria) is their primary bacterial endosymbiont and expected to provide its hosts with essential amino acids that are deficient in their plant sap diet. Using cophylogenetic analyses, Carsonella appeared to show strict and long-term cospeciation with its psyllid hosts, indicative of a long history of coevolution (Chapter 4). This association also allowed testing of phylogenetic relationships, based on psyllid and Carsonella DNA, of psyllid species with uncertain species assignment and highlighted the need for future taxonomic revision and potential collapse of several Cardiaspina species into fewer taxa. Furthermore, recent genome analyses of Carsonella and psyllid secondary bacterial endosymbionts has suggested that secondary endosymbionts may be required to complement Carsonella which is not able to provide the full suite of essential amino acids to its hosts. In this study, it was found that a secondary endosymbiont (Arsenophonus or Sodalis, both Gammaproteobacteria) was present at 100 % prevalence in 12 populations of Cardiaspina psyllids and one of the closely related Glycaspis. While cophylogenetic analyses indicated their coevolution with psyllids includes host switches and endosymbiont replacement, there were molecular patterns in two endosymbiont lineages that were characteristic of long-term host associations. Secondary endosymbionts of Cardiaspina appeared to have obligate relationships with psyllid hosts just as it was confirmed for their primary endosymbiont. This is possibly applicable to the entire superfamily Psylloidea. The principal natural enemies of psyllids, parasitoids belonging to the Psyllaephagus genus (Hymenoptera: Encyrtidae), were prominent in up to seven species of Cardiaspina psyllids and in one species of related Spondyliaspis (Chapter 5). Psyllaephagus appeared to be characterised by the presence of cryptic species. Diversification of Psyllaephagus was largely comprised of patterns of host specialisation and host switches between co-occurring hosts, while the generalist hyperparasitoid Coccidoctonus psyllae (Hymenoptera: Encyrtidae) codiverged with its primary parasitoid host complex suggesting potential ongoing speciation in this hyperparasitoid species. The high degree of specialisation suggested that the generalist strategy of parasitoids is likely to be rare even amongst closely related hosts, such as the Cardiaspina species of this study, and that parasitoid species richness is probably much higher than currently estimated. This PhD thesis has unravelled major factors and processes influencing population dynamics, community structure and biodiversity of Australian native psyllids that are of ecological significance due to their outbreak potential on Eucalyptus. Population dynamic studies of outbreaking species are important for predictions of future insect outbreaks, in particular as the frequency and intensity of insect outbreaks are expected to increase with climate change