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

<p>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.</p>

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

<p>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.</p>

Vascular epiphyte assemblage structure and distribution patterns in the south-temperate zone

<p>Vascular epiphytes, which are specialised to spend their entire life cycle within trees, are significant contributors to local ecosystem services. However, our current understanding of epiphyte distributions, co-occurrences, and general ecology lags far behind that of terrestrial plants. Furthermore, the majority of epiphyte research is undertaken in tropical forests, with comparatively few studies extending into temperate climates. As such, whether epiphytic plant assemblage structure varies geographically, or is influenced by area and isolation effects needs further scrutiny. In addition, how epiphytes are distributed in relation to host tree ontogeny and microclimates specific to south-temperate forests is poorly understood. Here, I attempt to bridge this gap by researching epiphyte distributions and assemblage structure in New Zealand, southern Chile, and Australia. In the first biogeographic study of epiphyte-host interactions, I determined if epiphyte-host network structure (i.e. nestedness, species co-occurrences, species specialisation) varied among New Zealand and Chilean temperate forests (Chapter 2). At the forest stand level, network structure was consistent with stochastic structuring, which suggests that dispersal and disturbances are important drivers of epiphyte distributions at a biogeographic scale. However, deterministic structure was observed in New Zealand networks with regards to nestedness (i.e. when specialists interact with generalists), which suggests that positive species interactions influence epiphyte distributions at a within-tree scale. Second, I determined whether the composition of plant communities residing in epiphytic birds’ nest ferns (Asplenium goudeyi) on Lord Howe Island, Australia, are influenced by fern size, isolation from a major propagule source and resident plant community richness (Chapter 3). Results suggest that plant communities are structured by dispersal. For one, there was a significant isolation effect on resident plant community richness. Additionally, wind-dispersed taxa were well represented in isolated ferns, while animal-dispersed taxa and taxa with no specific dispersal strategies were absent. This is the first study to test the combined effects of area, isolation and resident plant richness on epiphytic plant assemblage structure. Third, using Darwin’s geological theory of island ontogeny as a theoretical construct, I explored changes in epiphyte species richness throughout tree ontogeny (Chapter 4). Theoretical frameworks have helped bridge the gap between our understanding of vascular epiphytes and terrestrial plants, however, none have been implemented to guide investigations on epiphyte assemblage development. Based on the general features of island ontogeny, I found three stages of epiphyte assemblage development: (i) an initial stage where host trees are devoid of epiphytes, (ii) a second stage where trees acquire epiphytes into maturity, and (iii) a hypothetical stage where epiphyte assemblages follow a period of species decline following host tree mortality. In addition to these results, I found interspecific variation in the ontogenetic stage at which host trees become favourable for epiphyte establishment and the rate at which epiphyte assemblages develop. Lastly, I explored the systematic distribution of epiphytes and mistletoes in relation to microclimate gradients around the trunks of trees (Chapter 5). In addition, I tested the physiological responses of epiphytes and mistletoes to reductions in their most limiting resources to determine if the responses were consistent with their distribution patterns. The radial distributions of epiphytes and mistletoes were highly directional, and paralleled gradients of humidity, light and water. Additionally, the photochemical efficiency of epiphytes and CO₂ assimilation in mistletoe leaves decreased in plants growing in environments with lower water and light availability, respectively. However, mistletoe leaves still assimilated CO₂ in lower light conditions, which suggests a high plasticity of mistletoes to growing in a canopy environment. Despite over 120 years of recognising the importance of vertical microclimates on epiphyte distributions, this is the first systematic study of epiphytic plant distributions in relation to microclimate gradients around the trunks of trees. This thesis has increased our understanding of epiphytic plant assemblage structure, and how it is influenced by host tree species, isolation, area and resident plant species richness. In addition, this thesis has increased our understanding of the effect of host tree ontogeny and microclimate on epiphyte distribution patterns. Together, these studies may be built upon more broadly to further elucidate drivers of epiphyte assembly and distribution patterns.</p>

Vascular epiphyte assemblage structure and distribution patterns in the south-temperate zone

<p>Vascular epiphytes, which are specialised to spend their entire life cycle within trees, are significant contributors to local ecosystem services. However, our current understanding of epiphyte distributions, co-occurrences, and general ecology lags far behind that of terrestrial plants. Furthermore, the majority of epiphyte research is undertaken in tropical forests, with comparatively few studies extending into temperate climates. As such, whether epiphytic plant assemblage structure varies geographically, or is influenced by area and isolation effects needs further scrutiny. In addition, how epiphytes are distributed in relation to host tree ontogeny and microclimates specific to south-temperate forests is poorly understood. Here, I attempt to bridge this gap by researching epiphyte distributions and assemblage structure in New Zealand, southern Chile, and Australia. In the first biogeographic study of epiphyte-host interactions, I determined if epiphyte-host network structure (i.e. nestedness, species co-occurrences, species specialisation) varied among New Zealand and Chilean temperate forests (Chapter 2). At the forest stand level, network structure was consistent with stochastic structuring, which suggests that dispersal and disturbances are important drivers of epiphyte distributions at a biogeographic scale. However, deterministic structure was observed in New Zealand networks with regards to nestedness (i.e. when specialists interact with generalists), which suggests that positive species interactions influence epiphyte distributions at a within-tree scale. Second, I determined whether the composition of plant communities residing in epiphytic birds’ nest ferns (Asplenium goudeyi) on Lord Howe Island, Australia, are influenced by fern size, isolation from a major propagule source and resident plant community richness (Chapter 3). Results suggest that plant communities are structured by dispersal. For one, there was a significant isolation effect on resident plant community richness. Additionally, wind-dispersed taxa were well represented in isolated ferns, while animal-dispersed taxa and taxa with no specific dispersal strategies were absent. This is the first study to test the combined effects of area, isolation and resident plant richness on epiphytic plant assemblage structure. Third, using Darwin’s geological theory of island ontogeny as a theoretical construct, I explored changes in epiphyte species richness throughout tree ontogeny (Chapter 4). Theoretical frameworks have helped bridge the gap between our understanding of vascular epiphytes and terrestrial plants, however, none have been implemented to guide investigations on epiphyte assemblage development. Based on the general features of island ontogeny, I found three stages of epiphyte assemblage development: (i) an initial stage where host trees are devoid of epiphytes, (ii) a second stage where trees acquire epiphytes into maturity, and (iii) a hypothetical stage where epiphyte assemblages follow a period of species decline following host tree mortality. In addition to these results, I found interspecific variation in the ontogenetic stage at which host trees become favourable for epiphyte establishment and the rate at which epiphyte assemblages develop. Lastly, I explored the systematic distribution of epiphytes and mistletoes in relation to microclimate gradients around the trunks of trees (Chapter 5). In addition, I tested the physiological responses of epiphytes and mistletoes to reductions in their most limiting resources to determine if the responses were consistent with their distribution patterns. The radial distributions of epiphytes and mistletoes were highly directional, and paralleled gradients of humidity, light and water. Additionally, the photochemical efficiency of epiphytes and CO₂ assimilation in mistletoe leaves decreased in plants growing in environments with lower water and light availability, respectively. However, mistletoe leaves still assimilated CO₂ in lower light conditions, which suggests a high plasticity of mistletoes to growing in a canopy environment. Despite over 120 years of recognising the importance of vertical microclimates on epiphyte distributions, this is the first systematic study of epiphytic plant distributions in relation to microclimate gradients around the trunks of trees. This thesis has increased our understanding of epiphytic plant assemblage structure, and how it is influenced by host tree species, isolation, area and resident plant species richness. In addition, this thesis has increased our understanding of the effect of host tree ontogeny and microclimate on epiphyte distribution patterns. Together, these studies may be built upon more broadly to further elucidate drivers of epiphyte assembly and distribution patterns.</p>

Persistent Effects of Historical Selective Logging on a Vascular Epiphyte Assemblage in the Forest Canopy of the Western Ghats, India

Forest canopies have been dubbed the last biological frontier and continue to remain underexplored. Vascular epiphytes form a rich assemblage of plants within the forest canopy and apart from sustaining diverse taxa, they also fulfill critical ecological functions. Vascular epiphytes are particularly sensitive to perturbations of microclimate and microhabitat within the canopy, especially from anthropogenic changes such as logging. The forests of the megadiverse Western Ghats in India harbor a rich assemblage of vascular epiphytes, but their ecology has not been examined systematically. We compared the diversity, abundance, and composition of a vascular epiphyte assemblage between an unlogged and a historically selectively logged forest in the southern Western Ghats, India, and identified factors affecting the epiphyte assemblage. Canopies of 100 trees each in selectively logged and unlogged forests were accessed using the single-rope technique. We found 20 species of vascular epiphytes with the assemblage dominated by members of Orchidaceae. The diversity and abundance of epiphytes were significantly greater in the selectively logged forest. One host tree, Cullenia exarillata, supported the greatest number of epiphytes in both forest stands. The niche widths of epiphyte species, computed with host tree species as a resource, were similar between the two stands but a greater number of species pairs overlapped in the selectively logged forest. Overall, epiphyte abundance was negatively associated with unlogged forests. Host tree species, tree height, and presence of moss on branches were positively associated with the abundance of epiphytes. Despite being ecologically important, no study has thus far examined the impact of selective logging on the epiphyte assemblage in the Western Ghats. Our findings contribute to the knowledge of vascular epiphytes from South and Southeast Asia and set the stage for future research and conservation.

Identification and Evolutionary Characterization of Papillomavirus Sequences in New World Monkeys (Genera Sapajus and Alouatta) from Argentina

Objective: In this study, we investigated the occurrence of papillomavirus (PV) infection in non-human primates (NHP, Platyrrhine) of northeastern Argentina by using broad-spectrum PCR primers at the L1 gene. In addition, we conducted a phylogenetic and coalescence analysis of viral sequences to explore their evolutionary history and evaluate the co-speciation hypothesis in the context of primate evolution. Methods: We obtained samples of 57 individuals from wild and captive populations of Alouatta caraya, Sapajus nigritus and Sapajus cay. We assessed PV infection by PCR amplification with the CUT primer system and sequencing of 337 bp (112 amino acids) of the L1 protein. The viral sequences were analyzed by phylogenetic and Bayesian coalescence methods to estimate the age of the most common recent ancestor (tMCRA) with BEAST, v1.4.8 software. We evaluated viral/host tree congruence with TreeMap v3.0. Results: We identified two novel putative PV sequences of the genus Gamma- PV in Sapajus sp and Alouatta caraya (SPV1 and AcPV1, respectively). The tMRCA of SPV1 was estimated at 11,941,682 years before present (ybp) and that of AcPV1 at 46,638,071 ybp, both predating the coalescence times of their hosts: 6.4 million years (MYA) and 6.8 MYA, respectively. Based on the comparison of primate and viral phylogenies, we could not reject the null hypothesis that the PV tree is no more congruent with the host tree than a random tree would be (P>0.05). Thus, a model of virus-host coevolution was rejected. Conclusion: This study presents the first report of PV infection in Platyrrhine species from Argentina, expands the range of described hosts for these viruses, and proposes new scenarios for their origin and dispersal.

Insights into the Role of Fungi in Pine Wilt Disease

Pine wilt disease (PWD) is a complex disease that severely affects the biodiversity and economy of Eurasian coniferous forests. Three factors are described as the main elements of the disease: the pinewood nematode (PWN) Bursaphelenchus xylophilus, the insect-vector Monochamus spp., and the host tree, mainly Pinus spp. Nonetheless, other microbial interactors have also been considered. The study of mycoflora in PWD dates back the late seventies. Culturomic studies have revealed diverse fungal communities associated with all PWD key players, composed frequently of saprophytic fungi (i.e., Aspergillus, Fusarium, Trichoderma) but also of necrotrophic pathogens associated with bark beetles, such as ophiostomatoid or blue-stain fungi. In particular, the ophiostomatoid fungi often recovered from wilted pine trees or insect pupal chambers/tunnels, are considered crucial for nematode multiplication and distribution in the host tree. Naturally occurring mycoflora, reported as possible biocontrol agents of the nematode, are also discussed in this review. This review discloses the contrasting effects of fungal communities in PWD and highlights promising fungal species as sources of PWD biocontrol in the framework of sustainable pest management actions.