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.