Observational and model evidence for and against the dilution effectexamples from pathogens and parasites of wild rodents

Type

Student thesis: Doctoral ThesisDoctor of Philosophy

Original languageEnglish
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Award date2018
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Abstract

In disease ecology, the relationship between biodiversity and pathogen transmission is still under investigation. In particular, the dilution effect, namely that higher biodiversity decreases disease transmission, is currently the most debated eco-epidemiological theory in the context of multi-host pathogen systems. Mechanisms of dilution include transmission and encounter reduction, and susceptible host regulation. This study integrated empirical data and mathematical modelling to investigate the transmission of parasites and pathogens in Welsh wild rodent communities, as rodents are considered an ideal system to study multi-host parasite/pathogen transmission in the ecoepidemiological context. Rodents were live-trapped and faecal samples and ecto-parasites were screened for parasites and pathogens. Field data were used, where relevant, to parameterise models of infection that investigated the effects of parameter variation and community composition on pathogens with different transmission modes. The final aims were to provide additional knowledge on Welsh rodent communities, to identify rodentborne parasites/pathogens circulating in the sampling area, and to improve understanding of local transmission dynamics, testing the dilution effect through eco-epidemiological
modelling. The main results from the parasite and pathogen screening were: a. the observation of host heterogeneity in ecto-parasite and macroparasite prevalence and burden, with different host species contributing in different ways to the transmission pool; b. the isolation of Anaplasma phagocytophilum and Babesia microti in ixodid ticks; c. Bartonella spp. were isolated in fleas, B. rochalimae, notably, for the first time in the UK. The directly transmitted pathogen model outputs confirmed that reduced (or “diluted”) infection prevalence might not represent a true dilution effect to some hosts, since
prevalence could decrease simultaneously with the increase of infectious individuals. The model was effective in recognising susceptible host regulation via inter-specific competition and predation as the most important dilution mechanism. Modelling the two similar but different host-tick-pathogen systems showed that the parameters affecting the juvenile stages of the ticks were the ones most affecting pathogen transmission: crucial information to develop targeted control strategies. In the system with the more generalist vector, Ixodes ricinus, dilution effect was more significant and more dilution mechanisms were observed. The key parameters regulating transmission were also different between the two systems, but the dilution was observed only with regards to
infectious hosts, as more complex communities led to amplification of infectious nymphs, representing amplified human disease risk. With regards to the flea-borne Bartonella, force of infection and proportion of hosts transmitting vertically were the parameters most affecting transmission and degree of the
dilution, which occurred through the mechanism of regulation of susceptible hosts, providing evidence that community composition was crucial to the dynamics of pathogen transmission. The average flea burden of infested hosts was another important parameter, which was estimated from empirical data, demonstrating the importance of field data collection. Finally, in each system, the parameters most affecting pathogen transmission, were also the most uncertain. This study supported the idea that the dilution effect is not a universal principle, but it can be observed under certain conditions considering the appropriate epidemiological metric. Nonetheless, in the context of pathogen emergence risk factors were identified, especially alteration of biological communities caused by human disturbance. Hence, it may be more sensible to investigate local pathogen dynamics, gather data, and develop specific control
measures instead of trying to find a one-fits-all disease-diversity relationship. In conclusion, the eco-epidemiological approach, overcoming boundaries between disciplines, is crucial to investigate and control wildlife pathogens, to conserve biodiversity, and reduce human disease risk.

Keywords

  • dilution effect, vector-borne diseases, disease ecology, mathematical modelling, Bartonella