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