Wildlife–livestock interactions in animal production systems: what are the biosecurity and health implications?

Abstract

Increasing wildlife–livestock interactions enhance opportunities for pathogen transmission and biodiversity erosion. This increases the risk of emerging diseases in wildlife, livestock, and humans. Biosecurity measures are needed, but rethinking of livestock production in high biodiversity regions is also required. A cross-sectoral transdisciplinary approach is required for the effective management of risks at the wildlife–livestock interface. It is urgent to find models and approaches that allow a better balance between protein production and biodiversity conservation. The ongoing COVID-19 crisis has emphasized more than ever the relevance of wildlife as a potential source of pathogens for other species, including humans, and the potential importance that interactions with wildlife can have on global health. Nevertheless, in the veterinary world, the concept of wildlife as a potential reservoir and source of pathogens detrimental to livestock production and health has been known for centuries. Well-known examples of livestock diseases in which the interface with wildlife plays, or has played, an important role include rinderpest, avian influenza, foot and mouth disease (FMD), and African swine fever (ASF). Rinderpest, caused by a morbillivirus of the family Paramyxoviridae, is one of only two diseases that have been globally eradicated (the other being smallpox in humans), after having caused major disease outbreaks in domestic and wild artiodactyl species for centuries. After a globally coordinated eradication campaign, the World Organisation for Animal Health (OIE) and the Food and Agriculture Organization (FAO) of the United Nations announced in 2011 that rinderpest virus had been eliminated from livestock, thus declaring global freedom from this disease (Hamilton et al., 2017). Circulation of rinderpest virus in endemic regions in wild susceptible species was an important consideration in the eradication campaign, and lack of recognition of wildlife reservoirs was one of the factors to which failure of initial campaigns in the 1960s and 70s was attributed (Morens et al., 2011). Other diseases, such as ASF and FMD, are still endemic and expanding across different regions of the world. FMD is estimated to be endemic in 77% of the global livestock population, in Africa, Asia, and some parts of South America (OIE, 2021a) and ASF is becoming endemic in Africa, Europe, Asia, and some parts of Oceania (OIE, 2021b). Efforts to control or eradicate these diseases are challenging, particularly in those areas where wild reservoir hosts contribute to their maintenance and spread. African swine fever virus (ASFV) has been known for more than a century to be maintained in the soft tick-warthog sylvatic cycle in natural savannah environments in East and Southern Africa. Occasional interactions between ASFV-infected ticks and domestic pigs have facilitated the dissemination of several ASFV genotypes into the domestic pig value-chain in Africa and subsequently into other parts of the world (Dixon et al., 2020). During the currently ongoing pandemic of ASF, the wild boar population in Europe has played a central role in the propagation of the virus into new areas. While most ASF spread appears to occur within domestic pig populations due to anthropogenic factors, incursions of ASFV into low biosecurity domestic pig farming systems from wild boar are also important (Brookes et al., 2021). Likewise, transboundary spread of FMD in susceptible domestic livestock such as cattle and pigs is commonly mediated by anthropogenic factors, such as movement of infected livestock, or the feeding of infected products to susceptible species (Di Nardo et al., 2011). However, in East and Southern Africa, the African buffalo interface plays an important role in maintaining FMD virus (FMDV) strains and disseminating them to adjacent susceptible livestock populations (Jori and Etter, 2016). These examples provide only a snapshot illustration of the potential role of wildlife on livestock disease and demonstrate the importance of the wildlife–livestock interface. At a planetary scale, several factors act as major drivers of increased wildlife–livestock interactions at these interfaces (Magouras et al., 2020). Critical drivers include the need to feed an ever-increasing world human population, which has altered the way in which livestock are farmed, the way in which we interact with the ecosystem, and climate change. These drivers not only increase the intensity and frequency of interactions between wildlife and potential spillover populations (e.g., humans and domesticated animals such as livestock) but also facilitate new transmission pathways for potential emerging pathogens. Some of the impacts of these interactions have been well-described in the literature, particularly those affecting livestock production and health. However, these interactions can also have very significant and devastating effects on wildlife populations and the environment. Importantly, circulation of undetected pathogens in the domestic and wild animal compartments also provides opportunity for the development of potentially dangerous emerging infectious diseases. In this review, we provide an overview of the drivers of wildlife–livestock interactions and their potential impacts on terrestrial livestock production. We define wildlife as any domesticated or non-domesticated species that is free-ranging and does not depend on mankind for food or reproduction. In addition, we present and discuss the major tools and methods to reduce wildlife–livestock contact and to mitigate its health implications, including biosecurity measures and the approaches and potential solutions for improved cohabitation between livestock and wildlife to encourage biodiversity and reduce negative impacts such as disease spillover. The world human population is expected to increase by 2 billion people over the next 30 yr, from 7.7 billion today to 9.7 billion in 2050. It could reach a number close to 11 billion people around the year 2100 (Abel et al., 2016). To keep up with this galloping population increase, humanity is faced with the enormous challenge of producing enough protein to meet demand; consequently, protein production is expected to double by 2050. Animal products contribute approximately 67% of total global protein production (Baldi and Gottardo, 2017), and livestock enterprises represent the world’s largest land user, either directly through grazing or indirectly through the production of fodder and grains. This need for space inevitably leads to deforestation, and agriculture is considered responsible for the disappearance of 130 million hectares of tropical forests (equivalent to the size of Brazil) between 1990 and 2015. This process of habitat degradation to increase land for agriculture facilitates increasing areas of interaction between livestock present in these agricultural areas and wildlife inhabiting primary or secondary forest (Jones et al., 2013). In addition, although some mitigating activities are being implemented, livestock production especially cattle farming is a major contributor of carbon release to the atmosphere and subsequent global warming and climate change (Koneswaran and Nierenberg, 2008). Many infectious diseases are climate sensitive, especially vector-borne diseases because arthropod vectors alter their distribution ranges, introducing vector-borne diseases into new areas. In this manner, tropical vector-borne diseases are progressively expanding into temperate areas of the planet. For example, blue tongue virus, once only found in the tropics, has been expanding into Europe where it has affected European livestock for several decades (Jacquot et al., 2017) and other tropical viruses such as Rift Valley fever virus could follow (Chevalier et al., 2010) As well as facilitating large-scale changes in wildlife–livestock interactions by altering the distributions of livestock, wildlife, and the disease vectors, land-use change (and the livestock management practices that go with this) and climate change also facilitate localized interactions. For example, in arid and semi-arid landscapes, the scarcity of water generates increasingly important hotspots of interaction between wild and domestic species around water sources (Jori et al., 2021a). Pastoral and rangeland ecosystems are common areas for ruminant production where they are reared in large extensions. In these ecosystems, interactions between wild and domestic herbivores are particularly common around water or grazing resources (Figure 1). These situations are well known to facilitate the transmission and maintain the circulation of shared diseases between domestic and wild species in all regions of the world, including tropical, temperate, and pre-polar areas (Du Toit et al., 2017). In many resource-poor countries, the boundaries of protected areas are not clearly defined or rely on permeable physical barriers such as poorly maintained fences or seasonal rivers (Figure 2). Two examples of hotspots of interaction, where sympatric wild and domestic species are attracted by the presence of water or food resources: (a) Shared meadows between sheep and Alpine ibex (Capra ibex) in the Swiss Alps (Courtesy of M. P. Ryser-Degiorgis). (b) Shared pastures between sheep and wild camelids in Peruvian highlands (Photo: F.J.). Patchy or diffuse interface: the between a wildlife and livestock can be for example, a physical wildlife and livestock areas is affected by maintenance or such as in this (Photo: The of livestock also wildlife–livestock especially livestock are from free-ranging production systems at the known as farming especially in resource-poor to production in to with the to high or products (Figure In to countries, farming has very important and for the of and such as food source of source of agricultural agricultural and agricultural production and 2021). up a large of global in this livestock is very biosecurity and with wildlife species (Jori et al., 2021a). In to countries, for improved animal through as well as has the increase in production in systems that However, these systems allow contact with wild and and it to mitigating negative impacts such as the increased risk of of domestic animals to pathogens by wildlife, and et al., 2020). Two examples of free-ranging pigs in different (a) pig farming in (Photo: (b) In and other it is to pigs in farming is an increasing for the products (Photo: F.J.). The need to livestock production that increasing interactions between wildlife and livestock more important in the next decades as a impacts on livestock and wildlife populations some of these negative and which are in more The impacts of interactions at the wildlife–livestock interface. The size of the and compartments are of the in size of the and the impacts between wildlife and livestock of negative impacts of wildlife interactions on livestock production are well include and due to infectious diseases, impacts on people due to food disease or and or of livestock due to interactions. to infectious diseases, are many examples of wildlife species as reservoirs of pathogens that have a on livestock production (Figure In most of those the disease does not in the wildlife but can have devastating impacts on livestock include wild as reservoirs of avian viruses et al., wild as reservoirs of viruses for domestic et al., being to act as reservoirs of and the African buffalo that is well known as the major wild reservoir of (Jori and Etter, et al., 2021a). or of such reservoirs with susceptible livestock populations can outbreaks that can into as disease between spread can be due to ongoing transmission from wildlife or more anthropogenic factors such as movement of infected livestock or (Dixon et al., 2020). are the effects of animal of animals and also occur due to the of for or control In countries, and control measures can be to control infectious diseases such as FMD, and although be by (e.g., a between livestock and in the shared of the control of diseases such as FMD and ASF in the of an the and to animals are infectious disease outbreaks in a not only affected but can also have impacts on the of animals and animal products from that not directly due to but also subsequently due to of in the of the (Dixon et al., 2020). outbreaks of some transboundary animal diseases such as FMD or ASF can due to eradication of freedom and ongoing et al., different infectious pathogens between wild and domestic species in different (a) examples of pathogens between species and and (b) examples of pathogens shared by a of species more of transmission from a wildlife reservoir to livestock is found in tropical where the common not only it on the of livestock wildlife, and humans, but can also virus of of of cattle due to are estimated to occur across affected include of susceptible livestock, such as and population control to reduce the of the interface et al., As well as the of disease due to of and increased some diseases that have wildlife reservoirs are also (Magouras et al., 2020). of include and and disease is in livestock and humans. In some pathogens not in animals (e.g., and and more to and control and As pathogens in livestock species, this also provides opportunity for pathogen and thus increasing the of emerging diseases. is virus in pigs in in spillover from et al., 2013). The of interfaces of livestock with wildlife are factors in the of diseases, in this the large population of domestic pigs opportunity for circulation and of the virus and its to humans. important of the of biodiversity on livestock production is the process known as the et al., 2016). 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