Gray wolves as sentinels for the presence of Echinococcus spp. and other gastrointestinal parasites in France

Abstract

Over the past 30 years, the gray wolf population has recovered in France, initially to wolves from Italy passing through the Alps. The population is carefully monitored, but little information is available on their helminth fauna, which includes parasites of public health importance: Echinococcus multilocularis and Echinococcus granulosus sensu lato. Capitalizing on the availability of 911 fecal samples collected for the noninvasive genetic monitoring of French wolf populations, along with the intestines from 15 dead wolves, the presence of Echinococcus species among others helminth species was evaluated in French wolves. A copro-PCR approach amplifying a large spectrum of parasites was used for fecal samples while intestines were analyzed using SCT. The fecal occurrences of E. granulosus sensu stricto (2.4%) and E. multilocularis (0.3%), and indeedother parasitic species, are similar to those of other European wolf populations including Taenia hydatigena (7.2%), Taenia krabbei (2.4%), Uncinaria stenocephala (2.4%), Mesocestoides litteratus (1.9%), Taenia ovis (0.3%), Taenia multiceps (0.1%), and Toxascaris leonina (0.1%). The three most abundant species were also found in the intestines. Infections by E. granulosus sensu stricto are in accordance with the overlap of wolf pack areas and sheep breeding pastoral units. However, the wolf does not appear to play a significant role in the lifecycle of E. granulosus sensu stricto. The availability of this opportunistic fecal sampling of wolves in southeastern France means that they can be used as sentinels for the surveillance of E. multilocularis in the context of its southward expansion observed in recent years.

Keywords: Copro-PCR; Echinococcus granulosus sensu stricto; Echinococcus multilocularis; Gray wolf; Nematode; Taenia spp..

Graphical abstract

Fig. 1

Distribution of wolf fecal samples analyzed according to season and year.

Fig. 2

Spatial distribution of the 911 fecal samples collected from wolves (gray circle) in southeastern France submitted to copro-DNA analyses for identification of gastrointestinal parasites. The size of the circles is proportional to the number of samples collected per municipality. The departments (corresponding to NUTS3 level) are indicated by black lines.

Fig. 3

Location of the French wolf fecal samples positive for Echinococcus granulosus sensu stricto (green circles) and Echinococcus multilocularis (red circles). The E. multilocularis-positive fecal samples of dogs (red triangles) and wolves (small red diamonds) from Imperia (Italy) taken from Massolo et al., (2018) are also shown.

Fig. 4

Histogram of the total number of fecal samples analyzed for each French wolf pack with a minimum of 12 fecal samples available, with indication of the detection of cestodes (red), nematodes (orange) or absence of parasites (green).