Path analyses of cross-sectional and longitudinal data suggest that variability in natural communities of blood-associated parasites is derived from host characteristics and not interspecific interactions

BACKGROUND: The parasite composition of wild host individuals often impacts their behavior and physiology, and the transmission dynamics of pathogenic species thereby determines disease risk in natural communities. Yet, the determinants of parasite composition in natural communities are still obscure. In particular, three fundamental questions remain open: (1) what are the relative roles of host and environmental characteristics compared with direct interactions between parasites in determining the community composition of parasites? (2) do these determinants affect parasites belonging to the same guild and those belonging to different guilds in similar manners? and (3) can cross-sectional and longitudinal analyses work interchangeably in detecting community determinants? Our study was designed to answer these three questions in a natural community of rodents and their fleas, ticks, and two vector-borne bacteria. METHODS: We sampled a natural population of Gerbillus andersoni rodents and their blood-associated parasites on two occasions. By combining path analysis and model selection approaches, we then explored multiple direct and indirect paths that connect (i) the environmental and host-related characteristics to the infection probability of a host by each of the four parasite species, and (ii) the infection probabilities of the four species by each other. RESULTS: Our results suggest that the majority of paths shaping the blood-associated communities are indirect, mostly determined by host characteristics and not by interspecific interactions or environmental conditions. The exact effects of host characteristics on infection probability by a given parasite depend on its life history and on the method of sampling, in which the cross-sectional and longitudinal methods are complementary. CONCLUSIONS: Despite the awareness of the need of ecological investigations into natural host-vector-parasite communities in light of the emergence and re-emergence of vector-borne diseases, we lack sampling methods that are both practical and reliable. Here we illustrated how comprehensive patterns can be revealed from observational data by applying path analysis and model selection approaches and combining cross-sectional and longitudinal analyses. By employing this combined approach on blood-associated parasites, we were able to distinguish between direct and indirect effects and to predict the causal relationships between host-related characteristics and the parasite composition over time and space. We concluded that direct interactions within the community play only a minor role in determining community composition relative to host characteristics and the life history of the community members. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-015-1029-5) contains supplementary material, which is available to authorized users.