Summary
In Southern Africa, the African Swine Fever (ASF) sylvatic cycle presents a permanent threat for the development of the pig farming industry. Warthogs (Phacochoerus africanus) and bushpigs (Potamochoerus larvatus ), wild reservoirs of ASF are present in Ndumo Game Reserve (NGR), located in Northern KwaZulu Natal Province in South Africa and within 30 km of the locations of endemic ASF outbreaks in Mozambique where sylvatic disease transmission has been implicated. To assess if wild suids represent a risk of ASF virus spillover to domestic pigs in the neighbouring community, transect counts and fence patrols were conducted and camera traps were deployed in NGR to estimate wild suid abundance and incursions outside NGR boundaries. We searched for Ornithodoros ticks in 35 warthog burrows distributed across different NGR areas. Pig farmers (n=254) surrounding Mathenjwa Community were interviewed to gather information on interactions between domestic and wild suids and the occurrence of ASF. We conclude that NGR has established populations of bushpigs and warthogs, estimated at 5 and 3-5 individuals/km2 respectively. Both species move out of the reserve regularly (15.4 warthogs/day and 6.35 bushpigs/day), with a significant increase of movements during the dry season. Some farmers observed warthogs and bushpigs as far as 8 and 19 km from the reserve respectively, but no direct wild-domestic suids interactions nor any ASF outbreaks were reported. In addition, no soft ticks were found among the 35 warthog burrows. The absence of ticks in warthog burrows from NGR and the absence of reported outbreaks and familiarity with ASF in the surrounding farming area, suggest that a sylvatic cycle of ASF is at present unlikely in NGR. However, further research should be undertaken to confirm this by surveying a larger number of warthog burrows and monitoring potential antibodies in warthogs from NGR and domestic pigs in the neighbouring community.
Key words: African swine fever, bushpigs, domestic pigs, warthogs, sylvatic cycle, South Africa
Introduction
In Southern Africa, warthogs (Phacochoerus africanus ) and bushpigs (Potamochoerus larvatus) are considered as potential wild reservoirs of African Swine Fever (ASF). Warthog is found in open savannah habitats in most of Sub-saharan Africa and their densities range from 1–10 individuals/km² in protected areas (Cumming, 1975). The bushpig is mainly distributed in forested areas of eastern, southern and western central Africa with densities ranging from 1–10 individuals/km² in protected areas (Venter, Ehlers Smith, & Seydack, 2016). ASF is a highly infectious and hemorrhagic disease affecting exclusively domestic and wild suids, a significant threat to the pig industry worldwide (S Costard, Mur, Lubroth, Sanchez-Vizcaino, & Pfeiffer, 2013). In Africa, the virus is maintained in two epidemiological cycles: the sylvatic cycle, involving warthogs and bushpigs, and the domestic cycle involving domestic pigs. The disease can be transmitted by direct contact with an infected animal, its body parts or its secretions, or indirectly through fomites or contaminated food (Chenais, Ståhl, Guberti, & Depner, 2018). Warthogs do not become viraemic, apart from a brief period as young warthog piglets, and thus do not transmit the disease directly (Plowright, 1981; Thomson, 1985). Warthogs transmit ASF through soft ticks bites, with Ornithodoros moubata acting as a vector of the disease among warthogs, but also between warthogs and other suids species, particularly domestic pigs. These ticks are the natural reservoir maintaining the disease (Pereira de Oliveira et al., 2019). In the absence of Ornithodoros ticks, warthogs do not excrete sufficient amount of virus to transmit the disease horizontally to domestic pigs, therefore, the presence of warthogs is not enough to maintain a permanent source of virus in the environment (Ferran Jori & Bastos, 2009). The bushpig has been proven to be naturally resistant by experimental infection (Oura, Powell, Anderson, & Parkhouse, 1998). Previous studies suggest that bushpigs could have a potential role in the transmission of ASF (Okoth et al., 2013) because they have been occasionally found carrying the virus in different parts of Africa. Transmission of the virus through direct contact to susceptible domestic pigs has been proven in captivity (Anderson, Hutchings, Mukarati, & Wilkinson, 1998). However, their potential to maintain ASFV in its natural habitat and its transmission to domestic pigs has not been proven (Ravaomanana et al., 2011; Ståhl et al., 2014).
In Southern and East Africa, the maintenance of ASF in a sylvatic cycle linked to the presence and maintenance of ASF virus inOrnithodoros ticks in warthog burrows, represents a challenge for the development of pig farming in rural areas due to a constant risk of ASF spill over to domestic pigs (Quembo, Jori, Heath, Pérez‐Sánchez, & Vosloo, 2016). This can occur through direct physical or indirect contact between wild and domestic suids through the sharing of environmental resources such as soil, forage and water, facilitating disease transmission (Kock, 2005). ASF is a disease of global concern as it has the capacity to spread worldwide and can lead to severe socio-economic impact, both in areas where it is newly introduced and where it is endemic (Chenais et al., 2019). In South Africa ASF is a notifiable disease with a disease-free area and a control area defined in 1935 where ASF has been reported as endemic. Spread of ASF out of the control area should be notified internationally to the OIE and could result in an international ban of pigs and pork trade involving the disease-free area (OIE, 2011).
ASF is endemic in Mozambique, adjacent to areas with extensive subsistence pig farming in South Africa. The first laboratory-confirmed outbreak of ASF in Mozambique was reported in 1960. A number of outbreaks have since been observed around the country, including in the region south of Maputo, within 30 km of our study site. Though movements of domestic pigs from one province to the other played a role in disease transmission and spread, the sylvatic cycle was considered equally important particularly in the vicinity of conservation areas where warthogs and bushpigs are common (M. L. Penrith et al., 2007).
The complexity in the eco-epidemiology of this multi-host pathogen disease makes it hard to implement disease mitigation strategies. Among other factors, farming practices in neighbouring communities, the distance from the neighbouring community to a protected area (PA), the availability of resources in PAs, and the nature of the fence (surrounding PAs) stimulate wildlife-livestock interactions that promote the introduction and spread of diseases (Kukielka et al., 2016). Cowled and Garner (2008) argued that behaviour, animal density, distribution, contact rate, and habitat connectivity of both the vector and susceptible species are important for understanding how diseases are transmitted between wildlife and livestock. For ASF, the higher the wild suid density within a PA the greater the chances that some of the suids will get into contact, directly or indirectly, with domestic pigs. Also, the further wild suids move from the PA into farmland, the greater the risk of disease transmission. Pech and McIlroy (1990) argued that the movements of pigs increase the likelihood of contact between infected and uninfected pigs, and thus the spatial extent, and velocity of the spread of a disease.
Fencing has a long history in wildlife conservation and in many cases it has proven to be an effective tool for keeping wildlife out of specific areas, controlling animal movements and disease outbreaks (Durant et al., 2015). Fences are often deleterious to wildlife, preventing access to food and water as well as natural migration, but also to protect wildlife from human threats (Pirie, Thomas, & Fellowes, 2017). However, given that they undergo changes, fences probably do not work in the same way and with the same efficiency in all cases. Floods, breaks due to wildlife movement and damage due to theft are different factors increasing fence permeability. Therefore a fence requires regular inspection and maintenance (Ferran Jori et al., 2011).
This study aims to provide quantitative information about the potential presence of a sylvatic cycle at the wildlife livestock interface around Ndumo Game Reserve (NGR), which is part of the Lebombo Transfrontier Conservation Area, a transboundary conservation initiative including protected areas from South Africa, Swaziland and Mozambique. NGR is home to warthogs and bushpigs which play a role in maintaining and transmitting livestock diseases (Solenne Costard et al., 2009). Also, it is adjacent to a communal area with a substantial amount of farmed pigs, generating a wildlife-livestock interface. In addition, the reserve is within the boundaries of the ASF control zone in South Africa. That means the area is suspected to have a sylvatic cycle in which Ornithodoro s tick populations colonize warthog burrows, representing a permanent source of ASF. The reserve shares its borders with Mozambique where ASF is considered to be endemic. Understanding the extent to which wild suids from NGR interact with surrounding domestic pigs close to NGR is critical for the surveillance and control of ASF. Therefore, the specific objectives of our study were: i) to estimate the population size of warthog and bushpigs in NGR; ii) to assess the presence of ticks in warthog burrows from NGR; iii) to study the movements of wild suids between NGR and the adjoining farming areas and their potential interactions with domestic pigs.
Methodology