The community ecology of rabbit (Oryctolagus cuniculus) parasites

This thesis investigates aspects of the community ecology of rabbit parasites with particular emphasis upon the gut helminths, utilising a 23 (later extended to 26) year time series of rabbits and their parasites. A clearer understanding of parasite communities can lead to more effective biological control strategies. Rabbits are regarded as a serious pest species throughout Europe and the Antipodes and the use of the myxomatosis virus, as a biological control agent, has already been tried and failed. However, a clearer picture of the parasite community may offer future possibilities for control. Additionally, the rabbit is a good model for other grazing species, as it carries a similar gut helminth community. Drug resistance is an increasing problem in a wide range of parasites. A clearer appreciation of parasite communities could also aid in the search for effective and environmentally sound pathogen control strategies (e.g. via cross immunity or competition with benign species). Theoretical models have revealed the importance of aggregation to the stability of the host parasite relationship, to parasite evolution and to interspecific parasite interactions. A number of models have considered the effect of varying aggregation upon these dynamics with differing outcomes to those where aggregation was a fixed parameter. Here the stability of the distribution for each of the rabbit helminths was examined using Taylor's power law. The analyses revealed that aggregation was not a stable parameter but varied with month, year, host sex, host age, and host myxomatosis status. Evidence for the existence of interspecific parasite interactions in natural systems has been equivocal. Factors influencing parasite intensity were evaluated for the gut helminth. A network of potential interactions between the parasites was revealed. Only month was shown to be of greater influence on the community. Following, from the above analyses, a community model was constructed which incorporated both seasonal forcing and interspecific parasite interactions, with interaction mediated via host immunity. One unexpected emergent property was an interaction between the seasonality and the immune decay rate with slower immune decay resulting in a shift of the immune response out of phase with the species against which it was produced. The model was also used to assess the potential effects of two control strategies, an anticestodal and a single species vaccine. The vaccine had greater effects on the whole community than the anticestodal because of the immune- mediated interactions. The host is also an integral part of the community as the parasite dynamics are linked with that of their host. Therefore an assessment of the parasites' impact upon host condition and fecundity was also undertaken. This revealed a variety of positive and negative associations between the parasites and their host, with potential implications for future host control strategies. This study has shown that ignoring parasite-parasite or parasite-host interactions and interactions of both the host and the parasite with the external environment, could result in a poor description of the community dynamics. Such complexities need to be considered and incorporated into theory if future control strategies for either host or parasites are to be effective

Pathogen Interactions, Population Cycles, and Phase Shifts

Interspecific pathogen interactions can profoundly affect pathogen population dynamics and the efficacy of control strategies. However, many pathogens exhibit cyclic abundance patterns (e.g. seasonality) and temporal asynchrony between interacting pathogens has the potential to reduce the impact of those interactions. Here we use an extension of our previously published model to investigate the effects of cyclic abundance patterns on pathogen interaction. We demonstrate that for interactions mediated through host immunity, immune memory can maintain the impact of an interaction even when the effector pathogen abundance is low or the pathogen is absent. Paradoxically, immune memory can result in pathogens interacting more strongly when temporally out of phase. We find that interactions between species can not only alter pathogen abundance but can also result in changes to the temporal pattern of the affected species. We further demonstrate that this phenomenon may be observed in a natural host / pathogen data set. Given that there is both a continuing debate as to the relevance of pathogen interactions in natural systems and increasing concern regarding treatment of coinfections of veterinary and medical importance, both the discovery of this measurable shift in cycle in the empirical data and the mechanism by which we identified the shift are important. Finally, as the model structure used here is analogous to simple predator-prey system models we also consider the consequences of these findings in the context of that system

Endemic infection reduces transmission potential of an epidemic parasite during co-infection

Endemic, low-virulence parasitic infections are common in nature. Such infections may deplete host resources, which in turn could affect the reproduction of other parasites during co-infection. We aimed to determine whether the reproduction, and therefore transmission potential, of an epidemic parasite was limited by energy costs imposed on the host by an endemic infection. Total lipids, triacylglycerols (TAG) and polar lipids were measured in cockroaches (Blattella germanica) that were fed ad libitum, starved or infected with an endemic parasite, Gregarina blattarum. Reproductive output of an epidemic parasite, Steinernema carpocapsae, was then assessed by counting the number of infective stages emerging from these three host groups. We found both starvation and gregarine infection reduced cockroach lipids, mainly through depletion of TAG. Further, both starvation and G. blattarum infection resulted in reduced emergence of nematode transmission stages. This is, to our knowledge, the first study to demonstrate directly that host resource depletion caused by endemic infection could affect epidemic disease transmission. In view of the ubiquity of endemic infections in nature, future studies of epidemic transmission should take greater account of endemic co-infections

Predicting the effects of parasite co-infection across species boundaries

It is normal for hosts to be co-infected by parasites. Interactions among co-infecting species can have profound consequences, including changing parasite transmission dynamics, altering disease severity and confounding attempts at parasite control. Despite the importance of co-infection, there is currently no way to predict how different parasite species may interact with one another, nor the consequences of those interactions. Here, we demonstrate a method that enables such prediction by identifying two nematode parasite groups based on taxonomy and characteristics of the parasitological niche. From an understanding of the interactions between the two defined groups in one host system (wild rabbits), we predict how two different nematode species, from the same defined groups, will interact in co-infections in a different host system (sheep), and then we test this experimentally. We show that, as predicted, in co-infections, the blood-feeding nematode Haemonchus contortus suppresses aspects of the sheep immune response, thereby facilitating the establishment and/or survival of the nematode Trichostrongylus colubriformis; and that the T. colubriformis-induced immune response negatively affects H. contortus. This work is, to our knowledge, the first to use empirical data from one host system to successfully predict the specific outcome of a different co-infection in a second host species. The study therefore takes the first step in defining a practical framework for predicting interspecific parasite interactions in other animal systems

Infection history and current co-infection with Schistosoma mansoni decreases Plasmodium species intensities in pre-school children from Uganda

Malaria-schistosomiasis co-infections are common in sub-Saharan Africa but studies present equivocal results regarding the inter-specific relationships between these parasites. Through mixed model analyses of a dataset of Ugandan preschool children, we explore how current co-infection and prior infection with either Schistosoma mansoni or Plasmodium species, alter subsequent 1) Plasmodium intensity 2) Plasmodium risk and 3) S. mansoni risk. Co-infection and prior infections with S. mansoni were associated with reduced Plasmodium intensity, moderated by prior Plasmodium infections, wealth and host age. Future work should assess whether these interactions impact host health and parasite control efficacy in this vulnerable age group

Infection history and current co-infection with Schistosoma mansoni decreases Plasmodium species intensities in pre-school children from Uganda

Malaria-schistosomiasis co-infections are common in sub-Saharan Africa but studies present equivocal results regarding the inter-specific relationships between these parasites. Through mixed model analyses of a dataset of Ugandan preschool children, we explore how current co-infection and prior infection with either Schistosoma mansoni or Plasmodium species, alter subsequent 1) Plasmodium intensity 2) Plasmodium risk and 3) S. mansoni risk. Co-infection and prior infections with S. mansoni were associated with reduced Plasmodium intensity, moderated by prior Plasmodium infections, wealth and host age. Future work should assess whether these interactions impact host health and parasite control efficacy in this vulnerable age group

Breaking beta: deconstructing the parasite transmission function

Transmission is a fundamental step in the life cycle of every parasite but it is also one of the most challenging processes to model and quantify. In most host–parasite models, the transmission process is encapsulated by a single parameterβ. Many different biological processes and interactions, acting on both hosts and infectious organisms, are subsumed in this single term. There are, however, at least two undesirable consequences of this high level of abstraction. First, nonlinearities and heterogeneities that can be critical to the dynamic behaviour of infections are poorly represented; second, estimating the transmission coefficientβfrom field data is often very difficult. In this paper, we present a conceptual model, which breaks the transmission process into its component parts. This deconstruction enables us to identify circumstances that generate nonlinearities in transmission, with potential implications for emergent transmission behaviour at individual and population scales. Such behaviour cannot be explained by the traditional linear transmission frameworks. The deconstruction also provides a clearer link to the empirical estimation of key components of transmission and enables the construction of flexible models that produce a unified understanding of the spread of both micro- and macro-parasite infectious disease agents

Annual short-burst mass anthelmintic administration reduces tuberculosis severity but not prevalence in a wildlife reservoir

Introduction: Tuberculosis (TB), caused by the Mycobacterium tuberculosis complex (MTC), is an important disease in both human and animal systems. Helminths are commonly found in coinfection with MTC and TB is often exacerbated in such coinfections. Long-term anthelmintic administration, to control helminths, can improve a host’s ability to control MTC infection. Mass drug administration programmes, in which anthelmintics are given only once or twice a year, leaving periods where helminth reinfection can occur, are common in both human and domestic animal populations. To date, the effect of such intermittent control programmes on MTC infection and severity has not been explored. Methods: Here we investigate the consequences of a ten-day, annual, mass ivermectin administration on TB prevalence and severity in free-ranging juvenile and yearling (<2 years) wild boar (Sus scrofa). Results: This single annual anthelmintic treatment administered over six years reduced TB severity. Further, the proportion of wild boar with severe TB continued to decrease with successive treatments. TB prevalence, however, did not decrease significantly over the course of the study. Discussion: While ivermectin has direct anti-mycobacterial effects in vitro, the short duration of treatment means that the reduction in TB severity we observe in wild boar is unlikely to be accounted for by such a direct mechanism. Disruption of the helminth community and subsequent modification or enhancement of the host immune response is a potential mechanism. Future work should examine the consequences of annual anthelmintic drug administration on helminth community composition and structure and on the host immunological responses through time

Coinfection: Doing the math

A transmission model clarifies the effects of influenza on pneumococcal pneumonia and bridges the gap between individual animal experiments and human epidemiological dat