Ecological investigation of a new host-parasite relationship : Parelaphostrongylus odocoilei in thinhorn sheep (Ovis dalli)

Abstract

Discovery of a new host-parasite relationship, Parelaphostrongylus odocoilei in Dall’s sheep (Ovis dalli dalli) in the Canadian North, prompted the first investigation of the geographic distribution, pathogenesis, ecology and epidemiology of this parasite, as well as the related protostrongylid Protostrongylus stilesi, at Subarctic latitudes (60-65ºN). All protostrongylid parasites have an indirect life-cycle, where first-stage larvae are shed in the feces of a mammalian definitive host, penetrate the foot of a gastropod intermediate host, and develop to infective third-stage larvae. Protostrongylid larvae were recovered from over 2000 fecal samples from thinhorn sheep (Ovis dalli) and other hosts for P. odocoilei and P. stilesi across northwestern North America (38-69 ºN). Through novel application of molecular techniques to identify morphologically indistinguishable first-stage larvae, new records for P. odocoilei were established at 20 locations. This provided insight into the historical origins and biogeography of this new host-parasite relationship, and greatly expanded the known geographic range of both protostrongylids. Clinical effects, including a neurological syndrome, were described in five thinhorn sheep experimentally infected with P. odocoilei. Neural and respiratory pathology in these five sheep were compared with over 50 wild Dall’s sheep from a population naturally infected with P. odocoilei and P. stilesi. In the end stages, diffuse verminous interstitial pneumonia associated with P. odocoilei led to respiratory failure, and may have acted as a predisposing factor for bacterial pneumonia, which caused sporadic mortalities in this wild population. At Subarctic latitudes, seasonal patterns in host and parasite availability, including larval shedding by Dall’s sheep and larval development in experimentally infected gastropods, suggested that lambs become infected with P. odocoilei in a narrow seasonal window in their first fall on winter range. In combination with laboratory experiments, a degree day model for temperature-dependent larval development was developed, validated, and applied to describe and predict the effects of climate warming on protostrongylid parasites of thinhorn sheep in northern North America. In a future of climate warming, the narrow seasonal window for parasite development and transmission would be significantly extended, leading to amplification of populations of P. odocoilei and P. stilesi in endemic regions, and possibly range expansion of P. odocoilei. This may have consequences for the health of thinhorn sheep, as well as other wildlife that are important resources in the Canadian North.