Predator dietary response to prey density variation and consequences for cestode transmission

Abstract

The functional response of predators to prey density variations has previously been investigated in order to understand predation patterns. However, the consequences of functional response on parasite transmission remain largely unexplored. The rodents Microtus arvalis and Arvicola terrestris are the main prey of the red fox Vulpes vulpes in eastern France. These species are intermediate and definitive hosts of the cestode Echinococcus multilocularis. We explored the dietary and contamination responses of the red fox to variations in prey density. The dietary response differed between the two prey species: no response for M. arvalis and a type III-like (sigmoidal) response for A. terrestris that shows possible interference with M. arvalis. The fox contamination response followed a type II shape (asymptotic) for both species. We conclude that fox predation is species specific and E. multilocularis transmission is likely to be regulated by a complex combination of predation and immunologic factors. These results should provide a better understanding of the biological and ecological mechanisms involved in the transmission dynamics of trophically transmitted parasites when multiple hosts are involved. The relevance of the models of parasite transmission should be enhanced if non-linear patterns are taken into account.

Trophic ecology, behaviour and host population dynamics in Echinococcus multilocularis transmission

“…This place is located in the historical area of higher endemicity of Western Europe, and the average parasite prevalence in fox populations ranged from 20% to 65% (Raoul, Deplazes et al, 2001). Based on the copro-ELISA diagnostic on 1252 faeces collected in the field, Raoul et al (2010) showed that E. multilocularis infection in foxes was asymptotically related to both A. scherman and M. arvalis relative density in the field, suggesting a non-linear parasitic response: infection rose quickly up to a plateau that may be partly attributed to immunity mechanisms regulating infection level. In the Slovak Republic, 3096 red foxes were collected in the entire country between 2000 and 2004 and analysed for E. multilocularis infection using the sedimentation and counting technique (Miterpakova et al, 2006).…”

“…The existence of at least two density-dependent mechanisms acting on the control of the parasite transmission dynamics is described: one is based on the variations in the availability of resources including intermediate hosts (Rausch, 1995;Saitoh and Takahashi, 1998;Miterpakova et al, 2006;Tanner et al, 2006;Hegglin et al, 2007;Guislain et al, 2008;Robardet et al, 2008;Raoul et al, 2010;Stien et al, 2010;Wang et al, 2010;Liccioli et al, 2014), and the other is based on the variations in the density of the definitive host and in their faeces distribution (Ewald, 1993;Raoul et al, 2003;Guislain et al, 2007;Wang et al, 2010). However, we are clearly missing data to predict under which conditions the control of E. multilocularis transmission switches from being dominated by intermediate host density to being dominated by definitive host density, and vice-versa, in space and/or in time.…”

“…However, we are clearly missing data to predict under which conditions the control of E. multilocularis transmission switches from being dominated by intermediate host density to being dominated by definitive host density, and vice-versa, in space and/or in time. Additionally, the importance of considering non-linearity and both the direct and delayed response of definitive hosts contamination in relation to intermediate host population variations was noted in eastern France and Japan, respectively (Saitoh and Takahashi, 1998;Raoul et al, 2010).…”

Transmission ecosystems ofEchinococcus multilocularisin China and Central Asia

“…This may lead to phases of large population densities where the biomass of the total population of intermediate host can reach several tens of kilograms per ha. During those periods, fox definitive hosts feed almost exclusively on those prey populations that are easy to access and are more likely to ingest infected small mammals even when prevalence is low (Raoul et al 2010). These factors foster transmission (Giraudoux et al 2002) and human exposure risk (Viel et al 1999), the latter possibly via dogs feeding on abundant reservoirs of small mammal intermediate hosts close to towns, villages and rural settlements.…”

Egg intensity and freeze-thawing of fecal samples affect sensitivity of Echinococcus multilocularis detection by PCR

“…Ecological studies assessing the temporal and spatial factors affecting the prevalence of E. multilocularis in wild canids often rely on the analysis of fecal samples (e.g., Nonaka et al 1998;Raoul et al 2010). In order to provide reliable estimates of parasite prevalence and understand E. multilocularis transmission ecology, it becomes crucial to address limitations related to PCR testing of fecal samples as diagnostic tool.…”