Demographic stochasticity drives epidemiological patterns in wildlife with implications for diseases and population management

Abstract

Infectious diseases raise many concerns for wildlife and new insights must be gained to manage infected populations. Wild ungulates provide opportunities to gain such insights as they host many pathogens. Using modelling and data collected from an intensively monitored population of Pyrenean chamois, we investigated the role of stochastic processes in governing epidemiological patterns of pestivirus spread in both protected and hunted populations. We showed that demographic stochasticity led to three epidemiological outcomes: early infection fade-out, epidemic outbreaks with population collapse, either followed by virus extinction or by endemic situations. Without re-introduction, the virus faded out in >50% of replications within 4 years and did not persist >20 years. Test-and-cull of infected animals and vaccination had limited effects relative to the efforts devoted, especially in hunted populations in which only quota reduction somewhat improve population recovery. Success of these strategies also relied on the maintenance of a high level of surveillance of hunter-harvested animals. Our findings suggested that, while surveillance and maintenance of population levels at intermediate densities to avoid large epidemics are useful at any time, a 'do nothing' approach during epidemics could be the 'least bad' management strategy in populations of ungulates species facing pestivirus infection.

Figure 1

Map of Eastern Pyrenees showing for Pyrenean chamois the most studied hunting reserves in France and Spain (QGIS Development Team (2018). QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org). 1a: Alt Pallars-Aran National Hunting Reserve (NHR), Northern Sector; 1b: Alt Pallars-Aran NHR, Southern Sector (Boí); 2: Principality of Andorra; 3: Cerdanya-Alt Urgell NHR; 4: Cadí NHR; 5: National Game and Wildlife Reserve of Orlu; 6: Freser-Setcases NHR. In purple (cluster 2): severe outbreaks followed by quick population recovery and decrease in virus circulation^,. In yellow (cluster 3): outbreaks followed by decreasing trends or absence of population recovery and an endemic situation of the infection^,,. In grey: persistence of the virus without any negative impact on population size^,. See text and Figure 2 for the definition of clusters 2 and 3.

Figure 2

Evolution of population size (A) and seroprevalence (B) over simulation time for PAM clusters. Curves: model replications (400) of a scenario without management strategies and virus introduction in 1991, partitioned in three groups according to PAM algorithm (in blue: 220 replications in cluster 1, in purple: 140 replications in cluster 2, in yellow: 40 replications in cluster 3).

Figure 3

Contribution of model parameters to output variations and relative variation (in brackets) in each output induced by a 25% increase in each parameter. Parameters whose main effect or interaction with another parameter accounted for more than 5% of the output variance were retained. Parameters accounting for less than 5% of the output variance were grouped, and the sum of the contributions was equal to model R². Six aggregated outputs were analysed: for all replications, including those in which the infection had faded-out, we considered the probability of virus persistence 4 years after virus introduction and the time after virus introduction needed to reach a probability of 80% of virus extinction in the population; for replications where the virus persisted more than 4 years after virus introduction, we considered the median cumulative epidemic size in T and P animals over the simulation time, the median cumulative number of infection-related losses over the simulation time, and the mean seroprevalence 10 years after virus introduction. Parameter definitions can be found in Table 2.

Figure 4

Outputs for management scenarios with test-and-cull and/or vaccination. Time after virus introduction needed to reach a probability of 80% of virus extinction in the population (A) and difference in population size (ΔN) after 10 years of epidemic for replications where the virus persisted more than 4 years after virus introduction (B), in two cases: protected population (dotted line) vs hunted population (solid line), for four scenarios: test-and-cull alone (orange), a combination of test-and-cull and vaccination (light blue), ban on hunting (purple) and increased hunting (darker blue). For each case (i.e., protected vs hunted), the reference scenario (i.e., no management method implemented) is represented in dark grey. Here, we used a capture rate of 30% and high surveillance and carcass collection (Table 3).

Figure 5

Simplified conceptual model of Pestivirus spread (adapted from Beaunée et al.). Squares represent health states: S0, newborns and juveniles protected by maternal immunity, S, susceptible to infection, T, transiently infected, R, immune, Rg, immune females infected during pregnancy, P, persistently infected, and V, vaccinated. Solid horizontal arrows represent flows between health states (loss of maternal antibodies, infection, recovery, loss of acquired immunity, vaccination, and loss of vaccine-induced immunity). Solid vertical arrows represent natural mortality and disease-induced mortality for T and P. Dashed arrows represent births. See Supplementary Fig. S3 for the representation of the complete conceptual model.