In this study we combine field data and theory for a case study system to confirm the hypothesis that the presence of wolves can lead to a reduction in TB prevalence compared to when they are absent. Our findings indicate that wolf predation may contribute to TB control in wild boar, reducing TB prevalence and the release of MTC into the environment. These factors are likely to contribute to reduced levels of indirect transmission from the wild boar infection reservoir to other hosts. The results have wide-ranging implications that highlight how predation can play a key role in the control of infectious disease in multi-host systems.

It has been postulated that MTC transmission between wild and domestic hosts is mostly indirect, mediated by contaminated vegetation, water, mud, feed or other substrates18,55. Wild boar are the primary reservoir host for MTC in Spain with infection to other host species likely to be through indirect transmission in regions where multiple hosts overlap56. Wild boar are relatively long-lived57 and older age classes can mount a formidable defence against predation. Therefore wolves are likely to select generalised (severely infected) individuals (which are the class responsible for shedding pathogen to the environment55) or piglets (which is an age group more likely to suffer generalised infection58). Such selective predation has been suggested as a key mechanism which can decrease infection prevalence in prey3 and was shown to lead to reduced prevalence of prion disease in cervids without a dramatic decrease in their density10. Our field observations and model study show that there is a reduction in wild boar disease prevalence without a consequent reduction in wild boar density in regions where wolves might selectively target piglets and generalised wild boar. Our results indicate that the decrease in prevalence would be less pronounced if predation targeted all classes indiscriminately or if it targeted only piglets. Therefore, our results support previous findings3,10 that suggest the ability of predators to preferentially select the most infected prey may be key to their role in disease control. Moreover, our findings suggest that wolves could play a key role in TB control in wildlife reservoirs in Spain. In Asturias, the annual cost of compensation paid to farmers due to wolf attacks on their livestock (€1,016,860) is a quarter of the annual expenses of the cattle TB eradication scheme (€4,163,348; Regional Government 2014). The ecosystem service provided by predators in terms of disease control should form part of the debate when discussing the impact of predators since here wolves may be allies of farmers, rather than enemies.

In the absence of wolves (Fig. 3), wild boar numbers increase significantly. Model results indicate that there is a lag between the increase in wild boar growth and the increase in TB prevalence since the increase in infected individuals has a similar increasing trend to that of the overall population. This could explain the observation that TB prevalence in wild boar in the absence of wolves has remained relatively fixed. Note, however, that while TB prevalence in wild boar has remained constant the model predicts that the density of generalised wild boar and the presence of MTC in the environment increases throughout the study period. It is notable that the empirical findings for areas of Asturias in which wolves are absent show that there is a near five-fold increase in TB detected in cattle between 2000–2014. Our model provides an explanation for how a small percentage increase in prevalence coupled with a large increase in population density in a reservoir population may lead to a large increase in environmental contamination. This could explain the observed increase in cattle TB in these regions.

The model system was adapted to examine the potential impact of predation on disease control beyond the Asturias case study system (Fig. 4). In areas with high TB prevalence such as central and southern Spain, the observed prevalence of TB is 50% and an increased proportion of those infected exhibit generalised infection (58%). Since predators may select the most severely infected individuals there is the potential for predation to have a greater impact on disease control in such settings. More specifically, as there is a higher prevalence of generalised individuals, there will proportionately be more predation on these super-shedders and therefore the potential to have an exaggerated effect on removing the wild boar that are responsible for shedding the pathogen in the environment, thus having greater potential to reduce spillover to other wild and domestic hosts. In this scenario our model results show that predation by wolves does lead to an exaggerated reduction in disease prevalence while leading to an increase in overall population density and reduction in the level of environmental pathogen. This increase in wild boar density is a direct result of the decrease in TB prevalence as the mortality from predation is lower than disease induced mortality due to TB that was experienced in the absence of wolves. This emphasises the generality of our findings and further highlights the potential role of predators in disease control.

Previous theoretical studies that have shown that, in disease regulated populations, predation can reduce the force of infection and thereby decrease the density of infected hosts, increase the density of susceptible hosts and lead to an increase in overall population density3,10. Our model study shows that increased mortality from predation is approximately balanced by a reduction in disease-induced mortality. A key result is therefore that the prey population can be regulated by the disease, with consequent high prevalence in the prey species or at a similar density by a predator but with low disease prevalence. This finding highlights how restrictions to predator growth may have only minor impacts on prey density but a major detrimental impact on the prevalence of infection in prey species. The mechanism that underlies the compensatory balance between predation and disease induced mortality has recently been explained in systems subject to culling/harvesting59. Tanner et al.59 show that in systems that lack long-lived immunity to infection, population reductions from harvesting are compensated due to a population level release from disease-induced mortality. The compensatory effect increases as disease virulence increases and occurs for systems with density-dependent, frequency-dependent and environmental (free-living) modes of transmission. They explain how harvesting in systems that harbour virulent parasites can lower disease prevalence without significantly reducing, or indeed can increase population density. Our findings show how mortality from predation is compensated by a release from disease-induced mortality that can reduce TB prevalence and the potential spillover of infection to sympatric hosts29,30. Tanner et al.59 also show that in systems in which individuals develop long-lasting immunity following infection harvesting leads to a significant reduction in population density and an increase in infected prevalence and agree with theory that examines the impact of predation in systems with long-lasting immunity11. This highlights the necessity to understand the system specific host infection dynamics that are subject to predation or harvesting59,60,61.

Our results agree with earlier findings that the removal of a predator from a system that is regulated by both predator-prey interactions and virulent infection may increase disease prevalence and suppress prey abundance3,12,13. Our model results suggest that in the initial years of wolf removal wild boar density can increase and disease prevalence stays low. This may indicate that predator removal can be beneficial, however this is only a transitory state. When the wolf reaches sufficiently low numbers the disease is able to re-infect the increased abundance of susceptibles so that over time the population becomes regulated by disease rather than predation. This is accompanied by an increase in environmental contamination and risk of spillover to other wild and domestic hosts. This further highlights the complexity and potential negative consequences of predator removal and the need to consider disease status in predator management programmes.

Our modelling results show good agreement with the field data for our case study system. We expect our general findings relating to reduced prevalence of TB and compensatory growth of wild boar in the face of predation to be robust to changes in our model assumptions. The key requirement is that TB is virulent and individuals do not recover to develop long-lasting immunity59. There are however specific aspects where the model and field study disagree. The model differs from field data in that it predicts a prevalence of generalised individuals of 25–30% whereas existing data for Asturias suggests 16.7%43. However, this lower prevalence was derived from a small data set (1 out of 6 being reported as generalised) and recent results from Asturias (personal communication, unpublished findings by the Asturias Government) would now indicate a higher prevalence of generalised in closer agreement with model findings. Also, in areas with wolves the empirical results indicated that cattle TB stayed constant rather than declining. The model results indicated that there would be an increase in wild boar density, a reduction in TB prevalence in wild boar and a reduction in generalised infected wild boar and MTC in the environment, therefore reducing the risk of transmission of MTC to livestock. This can be explained by: firstly, the wildlife reservoir in the Atlantic regions of Spain is composed of two main hosts, wild boar and badger43, and wolves are not likely to significantly interfere with badger population dynamics; secondly, the wildlife reservoir contributes to MTC maintenance, but is not the only driver. In Spain, the relative contribution of wildlife to cattle TB breakdowns varies between regions depending on the epidemiological circumstances62,63. Cattle movements, for instance, are likely to contribute to TB maintenance64.

Our study has highlighted the potential of predation by wolves to reduce TB prevalence in wild boar and thereby reduce the risk of transmission from a key wildlife reservoir of infection. The model framework developed in this study was tailored to the wild boar TB wolf system but the underlying processes that represent the population and epidemiological dynamics are general and therefore we expect the results to apply more broadly. In particular, when predation can regulate a prey species that was previously regulated by virulent pathogens it is likely that infection levels will be reduced. Of course, care must be taken when considering the impact of generalist predators on disease control as they may also prey on alternative species that do not harbour virulent pathogens and therefore where mortality due to predation will not be compensated. Nevertheless, the potential of predators to control infection should be recognised more widely and be contrasted with the detrimental impact of predatory losses to domestic species. The beneficial role of predators should be given more prominence particularly given the need to manage conservation conflicts associated with predator re-establishment65.