Parasite invasion following host reintroduction: a case study of Yellowstone's wolves

Abstract

Wildlife reintroductions select or treat individuals for good health with the expectation that these individuals will fare better than infected animals. However, these individuals, new to their environment, may also be particularly susceptible to circulating infections and this may result in high morbidity and mortality, potentially jeopardizing the goals of recovery. Here, using the reintroduction of the grey wolf (Canis lupus) into Yellowstone National Park as a case study, we address the question of how parasites invade a reintroduced population and consider the impact of these invasions on population performance. We find that several viral parasites rapidly invaded the population inside the park, likely via spillover from resident canid species, and we contrast these with the slower invasion of sarcoptic mange, caused by the mite Sarcoptes scabiei. The spatio-temporal patterns of mange invasion were largely consistent with patterns of host connectivity and density, and we demonstrate that the area of highest resource quality, supporting the greatest density of wolves, is also the region that appears most susceptible to repeated disease invasion and parasite-induced declines. The success of wolf reintroduction appears not to have been jeopardized by infectious disease, but now shows signs of regulation or limitation modulated by parasites.

Figure 1.

A map depicting the spatial spread of mange across wolf pack territories over time (95% kernel density estimates based on ± three months location data surrounding the first date of a pack's infection). The timing of infection is represented by the colour of the pack territory, and grey pack territories are those that remained uninfected during the study. Letters correspond to pack data displayed in figures 2 and 4. The Northern Range within Yellowstone is delineated by the northern band of packs (B–L, S) on the map, and the Interior encompasses the remainder of the park to the south and west.

Figure 2.

Time series of pack sizes and mange prevalence (class 1, 2 or 3) corresponding to packs displayed on the map in figure 1. Pack size and prevalence estimates were conducted in March, July and November of every year since the invasion of mange. Packs U–X are not displayed on the map as they remained uninfected and had disappeared or were not located ± three months surrounding the last documented pack infection.

Figure 3.

The risk of a wolf pack becoming infected with mange (a) decreases with Euclidean distance to its nearest infected neighbour and (b) increases with the percentage of territory overlap with its nearest infected neighbour (95% CIs depicted by dashed lines). Infection events are given for packs at risk in relation to (c) distance to and (d) percentage territory overlap with a pack's nearest infected neighbour. The red line depicts a Lowess fit to the data, or the approximate probability of infection given distance or proportion territory overlap. Blue dots are points that lie at the top or the bottom fifth percentile of their distributions within the subset that either became infected or remained negative. Individual points reflect actual samples for distance and territory overlap. Euclidean distances and extent of territory overlap were calculated using GIS software (ArcGIS v. 9.0), and risks of infection were estimated using a Cox proportional hazards analysis (Program R, survival package).

Figure 4.

Mange status of radio-collared individuals within packs over time. Each horizontal line is an individual tracked over time with their mange status denoted each time they are observed. Individuals are grouped by pack, the letters of which correspond to the packs displayed in figures 1 and 2.

Figure 5.

(a) Minimum wolf population counts within Yellowstone National Park from 1995 to 2010 with outbreaks of canine distemper and the first detection of mange noted. (b) Annual pack growth rates (λ = pack size_t/pack size_t−1) of the (i) Northern Range and (ii) Interior regions of the park, 1998–2010. Lines connect individual packs and symbols are colour-coded to denote years in which CDV and severe mange (class 2 or 3) were detected (squares represent the absence of CDV data). When λ = 0, packs went extinct. The red line is a Lowess fit to all the data showing the general trend in pack growth rates over time.