Discussion
Understanding transmission pathways between hosts is an essential step to improve the control of infectious diseases. From that perspective, investigating the nature, frequency and drivers facilitating interactions between wild and domestic pigs in our study area seems an important step to understand the potential drivers for the emergence of OD in wild boar populations. Interactions between domestic and wild suids are becoming increasingly important for the scientific community due to the social success of outdoor pig farming in developed economies (Delsart, Pol, Dufour, Rose, & Fablet, 2020) and the awareness of shared pathogens between both populations , particularly considering the global spread of African swine fever (Boklund et al., 2020; Brookes et al., 2021; Viltrop et al., 2021). However, to characterize the risk factors associated with different types of interaction, it is necessary to understand the biology and behaviour of the animal populations involved and equally, the behaviour of stakeholders managing wild and domestic suids resources.
The results obtained during this study suggest that small scale outdoor farming initiatives are widespread in the Ardèche territory and that practices facilitating interactions between domestic pigs and wild boars, were widespread in the Ardèche department and with a significantly higher presence in the OD area than outside. A third of the farmers interviewed reported intrusions or attempts from wild boars to enter the farm, while 23% of them had observed some evidence of direct interactions. The location of farms more prone to those interactions appeared significantly associated with a forested habitat (p=0.025), a higher estimated density of wild boar (p=0.06), a low-to intermediate biosecurity index (p=0.0001).
Reports of hybrid litters in at least 5 farms confirmed the occurrence of sexual interactions. Incursions of wild boars in the farms were more frequently reported in autumn and winter (Fig. 4) than spring or summer. Autumn coincides with the most active reproductive season of male wild boars in Europe, reported between November and January (Drimaj et al., 2019). During this period, they can be easily attracted by sows on heat in outdoor farming paddocks, where they try to break in and mate with them (Malmsten, Jansson, Lundeheim, & Dalin, 2017; Wu et al., 2012). This seasonality of sexual interactions was also highlighted in another study in Corsica, which in France is possibly considered as an extreme case for wild boar / domestic pig interactions. In that case, 57% of the interviewed farmers (Jori et al. 2017) reported interactions between wild boars and domestic pigs and 70% of the sexual interactions were equally observed in autumn (Jori et al., 2017). Despite these figures are much higher, they also suggest that the level of interaction captured by our study is considerable and the number of identified situations facilitating direct and indirect interactions between wild and domestic suids and the potential transmission and circulation of shared swine pathogens is important.
It is likely that reported figures of interaction through questionnaires are underestimated for several reasons. First of all, an important proportion of them occur during night time and are difficult to be witnessed directly by farmers. In most cases, these interactions are detected by the observation of damages in the fence or the observation of crossbred offspring a few weeks later. Further studies using ecological tools (camera traps and /or telemetry devices with proximity loggers) should be implemented in order to confirm and better quantify wild boar incursions in the farms and document the potential occurrence of wild boar-domestic pig interactions in the study area (Kukielka et al., 2013; Triguero-Ocaña et al., 2021).
Other sources of bias such as recall bias could have influenced hunters’ responses. In fact, hunters struggled more than farmers to place the observed events in time. In addition, a third of farmers (9/30) expressed a certain mistrust towards the questionnaire, despite insisting that responses would be anonymous. The majority of farmers admitted having observed sexual or trophic interactions, mostly towards the end of the questionnaire, when a higher level of trust had been achieved. Certainly, the fear of sanctions from local authorities, could have induced underreporting of the frequency of interactions in the farms. Indeed, local animal health authorities can control the farms and engage substantial sanctions if the infrastructure is not up to standard. In addition, since sexual interactions reported were only those leading to the birth of hybrids, a certain number of interactions not resulting in cross bred offspring could have been underestimated.
Our study cannot confirm the hypothesis that interactions between wild and domestic suids are correlated and therefore, responsible for the emergence of OD in wild boar. However, the occurrence of factors facilitating those interactions in the OD were highly significant (Table 2). However, several risky practices such as the abandonment of waste in the wild, slurry spreading and presence of wild boars in the slurry spread area were found to be more common inside than outside the OD area. Slurry spread is considered a particularly risky practice in the context of bacterial contamination of the environment and indirect faecal-oral transmission of pathogens such as E. coli (Munch, Errebo Larsen, & Aalbæck, 1987). The results of the survey do not make it possible to assess the risks linked to the route by faecal contamination. Unfortunately, our sampled population was limited and our observed trends should be confirmed with a larger and more representative sample of farmers and hunters and a deeper analysis, asking farmers for information on the area and the location of the spreading area in particular. However, they characterize a situation in which interactions occur with a certain regularity, facilitating the circulation of shared pathogens between both suid populations. Actually, a recent molecular study on the samples collected from wild boar in the study area suggests that the strain of E. coli causing mortality in wild boars has circulated and evolved for a certain time in the wild boar population (Perrat et al., 2022). Despite its origins are likely to be in domestic pigs, research efforts in the area have not been able to identify the source of this E. coli strain to date. However, our study shows that in this area practices facilitating interactions and the spillover of pathogens from domestic pigs to wild boars are abundant and widespread.
Although our farm sample was small, the predominance of infrastructures allowing the incursion of wild boars into farms was important and widespread in the territory, including those areas with high estimated densities and favourable wild boar habitat. Indeed, in our results, an intermediate level of biosecurity appeared strongly correlated (P <0.05) with the risk of wild boar incursion and trophic interactions. In that respect it is important to underline that fences are expensive for farmers, and very often, if the farming surface is important, their maintenance across the whole perimeter can represent a serious financial constraint for the farmer. Nevertheless, in the context of the African swine fever threat, it is likely that French outdoor pig farmers will be confronted with the obligation of increasing biosecurity measures, and mediation processes might be required to facilitate their local acceptance and implementation (Gisclard et al., 2021).
Wild boars can thus become contaminated by ingestion of the remains of animals infected with several pathogens (Jori et al., 2017), including African swine fever or bovine tuberculosis (Carrasco-Garcia, Barroso, Perez-Olivares, Montoro, & Vicente, 2018). Strains of toxin producingE. coli are an important foodborne pathogen able to contaminate animal carcasses and intoxicate potential consumers (Brookes, Jordan, Davis, Ward, & Heller, 2016). In addition, E.coli has been proven to spill over between domestic pigs and wild boar populations sharing the same environment in experimental (S. Barth et al., 2017) and field conditions (S. A. Barth et al., 2018). Similarly, among hunters, half of them disposed the offal waste themselves by burying it underground which reduces the risk contaminating the environment. However, a third of them gave (10/30) the offal to their dogs and 7% of the farmers reported dropping offal waste in the environment. Many pathogens can be shared between different wild and domestic animal species through inadequate carcass waste management including bovine tuberculosis (Cano-Terriza et al., 2018), Aujezky’s disease (Charrier et al., 2018) and other feaco-oral transmitted pathogens such as OD.
Another distinctive result from our study was the reporting of free-ranging pigs with features of pot-bellied pig phenotype observed by 26% of hunters between 2013 and 2015. The practice of keeping and breeding pot-bellied pigs, frequent in many EU countries, was identified in 8 leisure states among the list of 230 registered farms. Complementary interviews with local authorities confirmed an escape incident with a farm of several specimens of pot-bellied pigs from in the study area in 2015. Considering that sexual interactions reported by hunters occurred around the town where this farm was located, the possibility of cross breeding between wild boars and pot-bellied pigs is a plausible scenario. The abandonment of exotic pets can have serious consequences for the environment (Lockwood et al., 2019) and this is also applicable in the case of pigs kept as pets (Soler et al., 2021). In many EU countries, there are numerous shelters organisations dedicated to the rescue of abandoned pot-bellied pigs specimens. Despite these incidents are in general poorly investigated, there is evidence that abandoned pot-bellied pigs have the capacity to form sounders that remain in natural habitats in Southern Europe and interact with wild boar populations increasing the population of hybrids. This is becoming a common phenomenon in many countries were pot-bellied pigs are sold as pets and has been currently described in rural areas of Southern and Northern Spain (Delibes–Mateos & Delibes, 2013; Soler et al., 2021). Based on our results, this kind of interaction is worth reporting in this study, to raise awareness about this phenomenon and encourage French and EU authorities to monitor this kind of incidents and their impact among wild boar populations.