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

Abstract

BackgroundThe 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.MethodsWe 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.ResultsOur 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.ConclusionsDespite 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 materialThe online version of this article (doi:10.1186/s13071-015-1029-5) contains supplementary material, which is available to authorized users.

Haemoplasmas in wild rodents: Routes of transmission and infection dynamics

“…To assess the probability of being infected by MHLB and the MHLB loads in the rodents’ blood collected during experiments 1, 3, 4 and 5 (designated as infection parameters), following Cohen, Einav, et al. (), 100–200 μl of blood was collected from the retro‐orbital sinus of each individual by capillaries immersed in 0.15% EDTA and was stored in EDTA blood collection tubes at −20°C until further molecular analyses. To assess MHLB infection parameters in fleas collected during experiments 1 and 2, fleas were collected from the rodent body and their DNA was extracted.…”

“…To assess MHLB infection parameters in fleas collected during experiments 1 and 2, fleas were collected from the rodent body and their DNA was extracted. DNA was extracted from blood samples (experiments 1, 3, 4 and 5) and flea‐regurgitated blood (Experiment 2) using a MoBio Bacteremia DNA Isolation Kit, following the manufacturer's instructions (Cohen, Einav, et al., ). DNA from fleas (experiments 1 and 2) and buccal swabs (Experiment 3) was extracted using a DNeasy Blood and Tissue Kit (Qiagen, Valencia, CA, USA; Hawlena et al., ).…”

“…Each rodent was infested by 100 MHLB‐negative S. cleopatrae fleas. S. cleopatrae is the most dominant ectoparasite infesting G. andersoni in the Negev Desert sand dunes and has the highest prevalence of MHLB among all G. andersoni ectoparasites (Cohen, Einav, et al., ). These fleas were all Bartonella ‐negative and part of our breeding core, which is maintained as previously described (Krasnov, Khokhlova, Fielden, & Burdelova, , ; Supporting Information, ).…”

“…M. turicensis ”; Dean, Helps, Jones, & Tasker, ; Lappin, Dingman, Levy, Hawley, & Riley, ; Museux et al., ; Willi et al., ), through rodent faeces (Willi et al., ; Woods et al., ) and through vertical transmission from female to offspring rodents (Almy, Ladd, Sponenberg, Crisman, & Messick, 2006; Fujihara et al., ; Harvey & Gaskin, ; Sasaoka et al., ). Regarding infection dynamics, our longitudinal field data suggest that MHLB have high persistency in G. andersoni ; 90% of the MHLB‐positive individuals were infected 4 months after the first sampling (Cohen, Einav, et al., ). However, due to the observational nature of that study, the possibility that these rodents had cleared the infection and were reinfected towards the second sampling period could not be rejected.…”

“…This hostile nature led scientists to consider blood as a sterile environment that possesses living organisms only during disease (Brooks, Carroll, Butel, & Stephen, ; Hall & Lyman, ; Motoshima et al., ). However, recent evidence points to more permanent blood bacterial residents such as Bartonella and haemoplasma (haemotropic Mycoplasma ) species, which may use red blood cells as their primary microhabitat (Cohen, Einav, & Hawlena, ; Cohen, Toh, Munro, Dong, & Hawlena, ; Gavish et al., ; Gutiérrez, Morick, Cohen, Hawlena, & Harrus, ; Gutiérrez, Nachum‐Biala, & Harrus, ). Revealing the mechanisms of these bacteria's transmission and persistence will shed light on the evolutionary strategies underlying host–parasite/pathogen coexistence and will have an applied aspect considering that some of these bacteria are pathogenic to wild animals and humans (Atif, ; Breitschwerdt & Kordick, ; Eisen & Eisen, ; Hoelzle, Zeder, Felder, & Hoelzle, ; Liang, Nelson, & Fikrig, ; Messick, ; Ogden et al., ).…”