Disentangling complex disease ecology networks: Using structural equation modelling to quantify the direct and indirect effects of deer on Lyme borreliosis hazard

Quantifying the strengths of interactions in complex vector-borne disease ecological systems is challenging. Yet, overcoming this challenge is fundamental for understanding the ecological mechanisms shaping disease hazard. Here we quantified the strengths of the hypothesised direct and indirect mechanistic pathways through which deer affect ticks and one of the Lyme borreliosis pathogens, Borrelia afzelii, by conducting a combined analysis of three previously published datasets from 39 sites across Scotland. Structural equation modelling revealed that, as predicted, deer had a strong positive overall effect (direct and indirect pathways combined) on questing Ixodes ricinus nymph density and a weak, non-significant, negative overall effect on B. afzelii prevalence. This resulted in an overall weak, non-significant, positive effect of deer on B. afzelii hazard (the density of infected nymphs), indicating that their negative effect on B. afzelii prevalence was weaker than their positive effect on questing nymph density. A key novelty of this study was being able to tease apart the direct and indirect pathways for each of these overall effects and demonstrating that they were primarily driven by direct mechanisms, such as deer driving nymph density. Although deer negatively affected rodent abundance, the hypothesised indirect pathways from deer to ticks and pathogen, acting through vegetation and/or rodents, were weak. This could result from low densities of rodents relative to deer in Scotland, consistent with Scotland having among the lowest nymphal Lyme borreliosis pathogen prevalences in Europe. Applying the methodological framework used in this study would be useful for teasing apart complex interactions in other vector-borne disease systems.