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>

Epidemiological Factors Associated With Caligus rogercresseyi Infection, Abundance, and Spatial Distribution in Southern Chile

Sea lice (Caligus rogercresseyi) are external parasites that affect farmed salmonids in Chile, and the scale of their sanitary and economic impact cannot be overstated. Even though space–time patterns suppose parasite aggregation, specific locations related to different infestation levels, as well as their associated factors across the geographic range involved, had not been investigated as of the writing of the present article. The understanding of the effects and factors entailed by the presence of C. rogercresseyi may be deemed a key element of Integrated Pest Management (IPM). In the present study, the multivariate spatial scan statistic was used to identify geographic areas and times of C. rogercresseyi infestation and to estimate the factors associated with such patterns. We used official C. rogercresseyi monitoring data at the farm level, with a set of 13 covariates, to provide adjustment within the analyses. The analyses were carried out for a period of 5 years (2012–2016), and they included three fish species (Salmo salar, Oncorhynchus mykiss, and Oncorhynchus kisutch) in order to assess the consistency of the identified clusters. A retrospective multinomial, spatial, and temporal scan test was implemented to identify farm clusters of either of the different categories of C. rogercresseyi infested farms: baseline, medium, and high, based on the control chemical threshold established by the health authority. The baseline represents adequate farm performance against C. rogercresseyi infestation. Then, production and environmental factors of the medium and high infestation farms were compared with the baseline using regression techniques. The results revealed a total of 26 clusters (p &lt; 0.001), of which 12 correspond to baseline, 1 to medium, and the remaining 13 to high infestation clusters. In general, baseline clusters are detected in a latitudinal gradient on estuarine areas, with increasing relative risks to complex island water systems. There is a spatial structure in specific sites, north of Los Lagos Region and central Aysén Region, with high infestation clusters and epidemic peaks during 2013. In addition, average weight, salmon species, chemotherapeutants, latitude, temperature, salinity, and year category are factors associated with these C. rogercresseyi patterns. Recommendations for an IPM plan are provided, along with a discussion that considers the involvement of stock density thresholds by salmon species and the spatial structure of the efficacy of chemical control, both intended to avoid the advance of resistance and to minimize environmental residues.

Antimicrobial Activity of Chitosan Oligosaccharides with Special Attention to Antiparasitic Potential

The global rise of infectious disease outbreaks and the progression of microbial resistance reinforce the importance of researching new biomolecules. Obtained from the hydrolysis of chitosan, chitooligosaccharides (COSs) have demonstrated several biological properties, including antimicrobial, and greater advantage over chitosan due to their higher solubility and lower viscosity. Despite the evidence of the biotechnological potential of COSs, their effects on trypanosomatids are still scarce. The objectives of this study were the enzymatic production, characterization, and in vitro evaluation of the cytotoxic, antibacterial, antifungal, and antiparasitic effects of COSs. NMR and mass spectrometry analyses indicated the presence of a mixture with 81% deacetylated COS and acetylated hexamers. COSs demonstrated no evidence of cytotoxicity upon 2 mg/mL. In addition, COSs showed interesting activity against bacteria and yeasts and a time-dependent parasitic inhibition. Scanning electron microscopy images indicated a parasite aggregation ability of COSs. Thus, the broad biological effect of COSs makes them a promising molecule for the biomedical industry.

Heterogeneity in transmission parameters of hookworm infection within the baseline data from the TUMIKIA study in Kenya

Background As many countries with endemic soil-transmitted helminth (STH) burdens achieve high coverage levels of mass drug administration (MDA) to treat school-aged and pre-school-aged children, understanding the detailed effects of MDA on the epidemiology of STH infections is desirable in formulating future policies for morbidity and/or transmission control. Prevalence and mean intensity of infection are characterized by heterogeneity across a region, leading to uncertainty in the impact of MDA strategies. In this paper, we analyze this heterogeneity in terms of factors that govern the transmission dynamics of the parasite in the host population. Results Using data from the TUMIKIA study in Kenya (cluster STH prevalence range at baseline: 0–63%), we estimated these parameters and their variability across 120 population clusters in the study region, using a simple parasite transmission model and Gibbs-sampling Monte Carlo Markov chain techniques. We observed great heterogeneity in R0 values, with estimates ranging from 1.23 to 3.27, while k-values (which vary inversely with the degree of parasite aggregation within the human host population) range from 0.007 to 0.29 in a positive association with increasing prevalence. The main finding of this study is the increasing trend for greater parasite aggregation as prevalence declines to low levels, reflected in the low values of the negative binomial parameter k in clusters with low hookworm prevalence. Localized climatic and socioeconomic factors are investigated as potential drivers of these observed epidemiological patterns. Conclusions Our results show that lower prevalence is associated with higher degrees of aggregation and hence prevalence alone is not a good indicator of transmission intensity. As a consequence, approaches to MDA and monitoring and evaluation of community infection status may need to be adapted as transmission elimination is aimed for by targeted treatment approaches.

On the mechanistic roots of an ecological law: parasite aggregation

Parasite aggregation, a recurring pattern in macroparasite infections, is considered one of the “laws” of parasite ecology. Few hosts have a large number of parasites while most hosts have a low number of parasites. Phenomenological models of host-parasite systems thus use the negative-binomial distribution. However, to infer the mechanisms of aggregation, a mechanistic model that does not make any a priori assumptions is essential. Here we formulate a mechanistic model of parasite aggregation in hosts without assuming a negative-binomial distribution. Our results show that a simple model of parasite accumulation still results in an aggregated pattern, as shown by the derived mean and variance of the parasite distribution. By incorporating the derived statistics in host-parasite interactions, we can predict how aggregation affects the population dynamics of the hosts and parasites through time. Thus, our results can directly be applied to observed data as well as can inform the designing of statistical sampling procedures. Overall, we have shown how a plausible mechanistic process can result in the often observed phenomenon of parasite aggregation occurring in numerous ecological scenarios, thus providing a basis for a “law” of ecology.

Bat flies aggregation onArtibeus planirostrishosts in the Pantanal floodplain and surrounding plateaus

For parasites in natural systems, the most common pattern of spatial distribution is aggregation among hosts. The main causes of such aggregation are variable exposure of hosts to parasites and heterogeneity in host susceptibility. The objective of this study was to determine if there are differences in the aggregation pattern of two species of ectoparasitic flies between the Pantanal and Cerrado regions of Brazil on the batArtibeus planirostris.We collected the ectoparasites from bats captured between 2002 and 2017 with mist nets in 21 sites in the Pantanal and 15 sites in the surrounding plateaus. The results showed that the aggregation of ectoparasitic flies in Pantanal was more pronounced than in Cerrado. The discrepancy aggregation index (D) of the bat flyMegistopoda araneawas 0.877 in Pantanal and 0.724 in Cerrado. The D values ofAspidoptera phyllostomatiswas even higher, with 0.916 and 0.848 in the Pantanal and Cerrado, respectively. Differences in the shelters used may be the main factor shaping variation in aggregation, since the Pantanal does not have rock formations, with only foliage, crowns and hollow tree trunks. These differences likely affect host exposure to the parasites, leading to an increase in parasite aggregation.