Tri-trophic interactions of a predator-parasite-host assemblage in New Zealand

Parasites are ubiquitous and the antagonistic relationships between parasites and their hosts shape populations and ecosystems. However, our understanding of complex parasitic interactions is lacking. New Zealand’s largest endemic moth, Aenetus virescens (Lepidoptera: Hepialidae) is a long-lived arboreal parasite. Larvae grow to 100mm, living ~6 years in solitary tunnels in host trees. Larvae cover their tunnel entrance with silk and frass webbing, behind which they feed on host tree phloem. Webbing looks much like the tree background, potentially concealing larvae from predatory parrots who consume larvae by tearing wood from trees. Yet, the ecological and evolutionary relationships between the host tree, the parasitic larvae, and the avian predator remain unresolved. In this thesis, I use a system-based approach to investigate complex parasite-host interactions using A. virescens (hereafter “larvae”) as a model system. First, I investigate the mechanisms driving intraspecific parasite aggregation (Chapter 2). Overall, many hosts had few parasites and few hosts had many, with larvae consistently more abundant in larger hosts. I found no evidence for density-dependent competition as infrapopulation size had no effect on long-term larval growth. Host specificity, the number of species utilised from the larger pool available, reflects parasite niche breadth, risk of extinction and ability to colonise new locations. In Chapter 3, I investigate larvae host specificity in relation to host nutritional rewards (phloem turnover and phloem sugar content) and host defences (bark thickness and wood density). The number of species parasitized was not explained by tree abundance, nutritional rewards or wood density. However, the number of trees parasitised declined significantly with increasing bark thickness indicating host external defences are an important driver of host specificity. Camouflage in animals has traditionally been considered an anti-predator adaptation. Yet the adaptive consequences of camouflage, i.e. increased survivability via predator avoidance, has rarely been tested. In Chapter 4, I show that larvae webbing is visually cryptic to predating kaka, yet did not protect larvae from attack. Instead, cryptic webbing aids larvae thermoregulation suggesting crypsis is non-adaptive. These results support an exciting newly emerging paradigm shift that indicates the evolution of camouflage in animals may be more to do with abiotic conditions than biotic signalling. Males are often the “sicker sex”, experiencing higher pathogen and parasite loads than females. In Chapter 5, I construct the largest host-parasite database to date, spanning 70 animal and 22 plant families, from which I conduct a meta-analysis testing for male biased susceptibility (MBS). Then, I develop a theoretical model that explain MBS as a result of parasite-offspring competition for female resources. I present the first, unified model that explains male-biased susceptibility in animals and plants and provide parameters for model replication, applicable to almost all host-parasite pairings on Earth. This thesis presents the first investigations of the natural history of Aenetus virescens larvae, their relationships with host trees, and the interactions with their avian predator. The results herein support existing theories of parasite aggregation and host specificity from a novel perspective. Furthermore, results support a newly emerging paradigm shift in animal camouflage evolution, and suggest a unified explanation for male biased susceptibility in animals and plants. The results herein help further our understanding of complex antagonistic relationships between parasites and their hosts, presenting novel theories on which future research can be built.