African Swine Fever threatens Southeast Asia’s 11 endemic wild pig species

The spread of the most recent African Swine Fever (ASF) outbreak in Asia since late 2018 poses a significant threat to endemic pig species and socioeconomic security. Within domestic pigs and free-living Eurasian wild boars (both Sus scrofa ) in Asia, ASF causes almost 100% case fatality. The ongoing ASF epidemic has so far caused the death of over one hundred million domestic pigs, caus-ing unprecedented economic impacts on the global pork industry. Transmission among free-living wild boars has been reported, and transmission to threatened Asian pig species is probable but lacks research. Our assessment reveals a near-term risk for Southeast Asia’s 11 endemic pig species, which have small population sizes and small ranges that may be insufficient to withstand the initial, lethal onslaught of the disease. The decline of pigs also triggers cascading impacts for endangered carnivores, plant communities, and livelihoods of millions of people. Our management recommendations include time-critical research themes, improved emerging infectious disease detection through site-based monitoring and surveillance paired with online reporting and proper carcass disposal.

has) reached many of the region's threatened pigs. We then summarize factors contributing to the susceptibility of endemic pig species to ASF if it arrives in a region or island. We separate domestic and wild Sus scrofa, which is known to be affected by ASF, from the 11 threatened pig species for which there is no information about their susceptibility to ASF (Table 1). We assess the risk to specific species by considering the additional factors that could mediate local ASF transmission. This includes connectivity amongst regions or local religious prohibitions on pork consumption, which would lower the risk of native pigs being exposed to ASF, versus the presence of domestic pig husbandry or invasive Sus scrofa, which may increase the risk of being exposed to ASF.
The full severity of emerging infectious disease outbreaks and their potential cascading impacts are often underestimated (Lippi, Sanchi-Gomar, & Henry, 2020). Many countries lack adequate mitigation measures to prevent and control outbreaks in humans or animals, as suggested by patterns of delayed interventions, inadequate human health and veterinary care systems, and lack of cross-sectoral coordination to address human and animal health issues (Emanuel, 2020;Lippi & Plebani, 2020). Further, many institutions downplay or do not prepare for "tail-risks," an economic term defined as highly unlikely events that can have severe consequences (Acemoglu, Ozdaglar, & Tahbaz-Salehi, 2017). For example, the impacts of ASF in China have exceeded one trillion yuan (> $140 billion USD; Huang, 2020) and reduced calorie availability to people by 1-1.6% (Mason-D'Croz et al., 2020). The unexpected economic and human health impacts in China may foreshadow dire conservation problems in the rest of Asia. Specifically, the ongoing ASF epidemic poses an extinction threat for Asia's rarest pig species and the decline of wild pigs more generally will alter the forest ecology and cause socioeconomic impacts throughout the region.

ASF in domestic pigs
Domestic pigs (Sus scrofa) face almost 100% case fatality from ASF in Asia (Perez, Brihn, & Perez, 2019;FAO, 2020;USDA, 2020). The rapid spread of ASF in domestic pigs through mainland Asia started in northern China in August 2018 and moved south to Vietnam by February 2019 and the Philippines (Luzon Island) by July 2019 (Figure 1;FAO, 2020;Sur, 2019). Since late 2018, more than 100 million domestic pigs have died from the disease or been culled in China in an attempt to limit the spread of ASF (FAO, 2020). Almost all other Southeast Asian countries have now reported cases in domestic pigs. The disease has spread to northern India, south through Indonesia, east to the Philippines and Papua New Guinea, and now encompasses the range of rare warty pigs, pygmy hogs, and babirusa species (Figure 2; FAO, 2020;Sur, 2019;Zhong, 2020). We note that our abilities to track ASF is influenced by each countries' surveillance, testing, and reporting abilities, and this is often politically motivated. Therefore, ASF reporting is often unreliable and not comparable between countries.

ASF in wild Sus scrofa
The most common and widespread native pig in the region is the wild boar, which is listed as Least Concern for conservation by the IUCN Red List (Keuling & Leus, 2019). In previous outbreaks in Europe, the disease caused significant mortality of free-ranging wild boars (Chenais et al., 2019). In the 2007 outbreak, ASF spread to wild boars across Eurasia and to Madagascar and caused an initial epidemic phase with high fatality before becoming endemic with low transmission and mortality rates (Chenais et al., 2019;Schulz et al., 2019). ASF was eradicated from the Iberian Peninsula following intense control measures, but it remains endemic in Europe despite significant management efforts (Costard et al., 2013). ASF is already spreading among free-living wild boars in Asia (Guberti, Khomenko, Masiulis, & Kerba, 2019; FAO 2020; Figure 2). For example, South Korea has deployed snipers and drones to kill wild boars crossing from North Korea in its efforts to limit the spread of ASF (Zastrow, 2019). However, there has been no targeted research on the transmission of ASF to and among free-ranging native wild boars in Asia, so the extent and prevalence remains unknown (Vergne, Guinat, & Pfeiffer, 2020). The outbreak may be widespread given the infectiousness and rapid spread of ASF among domestic Asian pigs that are genetically similar to wild boar (Frantz, Haile, & Lin, 2019). Further, the spread of ASF from domestic to wild boars in Asia is also aided by the lack of biosecurity measures of "backyard" pig production throughout the region, which is known to be a risk factor in other regions (Cwynar, Stojkov, & Wlazlak, 2019;Wang, Sun, & Qiu, 2018). The spread of ASF in free-ranging pigs is certainly underreported because of the chronic lack of resources devoted to monitoring wildlife diseases in the region, especially given recent COVID-19-associated fieldwork limitations, as well as political reasons for intentionally TA B L E 1 Summary of risk factors potentially associated with ASF for Asian endemic pig species. ASF already affects wild and domestic Sus scrofa.
We did not include the presence of ticks that could transmit ASF because little is known about this for Southeast Asia. Note that conservation status is provided for the readers' reference and was not included in assessing threat of ASF infection Species Also present in Peninsular Malaysia.

F I G U R E 1 Timeline of African Swine Fever spread in Asia and domestic pig deaths (not culled).
Yellow points denote time of first positive ASF case in domestic Sus scrofa reported for each country, purple stars show when ASF was first reported in wild boars in each country. The orange spline shows smoothed temporal trend. Pig deaths come from incidences reported to the World Organisation for Animal Health (their widely used acronym is OIE) and do not include the deaths from culling of domestic pigs implemented to prevent the spread of ASF, which is estimated to exceed 100 million. The deaths reported are influenced by each countries' surveillance, testing, and reporting abilities, and thus should only be used to assess general trends. This graph illustrates that ASF pig mortality is increasing over time, but the threats to wild Sus scrofa and endemic pig species remain largely unknown underreporting (Vergne et al., 2017;Zhong, 2020). There are also few clear channels for sending samples or even communications to relevant authorities Vergne et al., 2020). Integrating these risk factors means that ASF will likely remain endemic among freeliving wild boars in Asia for the foreseeable future (Vergne et al., 2020).

ASF IN ENDEMIC ASIAN PIG SPECIES
Eleven other endemic Asian pig species are at risk from ASF. Currently, there has been no direct testing of whether ASF can spread to other Asian pig species but relevant epidemiological research on ASF suggests this is highly likely (Netherton, Connell, Benfield, & Dixon, 2019). ASF can infect at least five pig species from four genera (Netherton et al., 2019). In Africa, ASF infects common warthog (Phacochoerus africanus), bushpig (Potamochoerus porcus), and giant forest hog (Hylochoerus meinertzhageni) with frequent spillover events to domestic pigs (Penrith & Vosloo, 2009). Previous exposure to ASF or many other viral diseases is highly unlikely for any of Asia's isolated and insular endemic pig species, further reducing the likelihood of disease resistance. Many of the region's pigs in the Sus genus (warty pig and bearded pig species) interact or interbreed with wild, invasive, or domestic Sus scrofa (Melletti & Meijaard, 2017) and Southeast Asian pigs in the Sus genus have been predicted to be similarly susceptible to ASF as Sus scrofa (Netherton et al., 2019). There are also numerous tick species in Asia and since these are F I G U R E 2 The spread of African Swine Fever threatens Southeast Asia's 11 wild pig species. Hotter transparent colors correspond to larger outbreaks (more pigs infected) as of early August 2020 (1). The ranges of wild pigs species in Asia are shown with solid colors (4). Letter codes within the pig species legend (colors) denote IUCN threat level, listed here in increasing order: Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN), Critically Endangered (CR). Risk was qualitatively assessed by indicators shown in Table 1 rarely host specific, they may serve as a vector between pig species and ticks may also act as a reservoir that increase viral persistence (since some ticks live > 1 year; Golnar et al., 2019). However, there is no research on Asian ticks' ability to transmit ASF specifically, so this is speculative, and ticks were not included in our species-level risk assessments. Taken together, there is a high chance that Asia's endemic pigs will be exposed to ASF and as there is little evidence suggesting they would be immune to ASF.
In lieu of targeted research on this subject, it is prudent as a precautionary measure to consider that Asian wild pig species would be infected and impacted by the ASF virus (Vergne et al., 2020). We have thus established that ASF has or will likely arrive in areas with threatened endemic pigs that it can likely infect these species, and next we assess the likelihood it will infect endemic pigs.

Assessing risk
Unlike the previous outbreaks in wild boar where ASF became endemic and did not cause local extinctions, Asia's endemic pig species have dramatically smaller populations and smaller ranges that may be insufficient to withstand the initial and lethal onslaught of the disease. We assessed the threat of ASF on wild pig populations by assuming that transmission was possible and its likelihood was correlated with the contact frequency with pork production (pig farming), pork products, and international trade (Figure 2). The virus can spread via processed cooked or frozen products manufactured in China, so we included trade as a risk factor (CNN, 2020; FAO, 2020). We scaled threat of ASF from trade by overall trade connectivity, the number of pork-consuming people within the range of each pig species, and we also assessed whether pork production (pig husbandry) was common within each species range (see Table 1 for details on methods). Exposure to pork trade and thus ASF may be lower where the majority population follows Halal practices that forbid pork production and consumption, such as in the predominantly Muslim areas of Peninsular Malaysia, Brunei, Indonesia, and the southern Philippines (Luskin, Christina, Kelley, & Potts, 2014). However, we accounted for pork-consuming Buddhist or Taoist Chinese minority populations are found throughout the region, as well as Christians and animists in Kalimantan, North Sumatra, Sulawesi, and other Indonesian smaller islands such as Bali and East Nusa Tenggara. Finally, we assumed the presence of Sus scrofa would also facilitate transmission to other species through direct interactions, tick vectors, or if other endemic pig species foraged on infected Sus scrofa carcasses. We qualitatively scored each of these threat factors from low (score = 1), medium (score = 2), high (score = 3), and very high (score = 4), and then summed their scores to produce an overall threat level for each species. Scoring was assessed by four assessors of the IUCN Red List for Suidae and based on information gathered by a literature review.
To date, ASF has spread to the Indonesian provinces of East Nusa Tenggara and North Sumatra, all of which have strong local cultures of pork production and consumption and high frequency of international trade (Table 1; FAO, 2020). Thus, the transmission of ASF to wild Sus scrofa in these locations was likely, while in Sumatra, there is also the potential for transmission to the sympatric subspecies of bearded pig (Sus barbatus oi), whose population is already at higher risk than the Bornean subspecies (Sus barbatus barbatus) due to habitat loss (Ke & Luskin, 2019). These ASF hotspots in Indonesia are well connected to Java, Kalimantan and Sulawesi by dozens of daily boat, plane and car-ferry travel routes. This is especially concerning for the Javan and Sulawesi warty pigs (Sus verrucosus and Sus celebensis, respectively) and Sulawesi's babirusa (Babyrousa celebensis). Sulawesi is at a particularly high-risk because of its strong culture of pig production and consumption, and its prevalence of wildlife hunting and markets (Latinne et al., 2020), where zoonotic diseases may emerge and spread. The Togian islands are more accessible than Sula and Buru islands, so the risk for Togian babirusa (Babyrousa togeanensis) is higher (medium) than to Hairy babirusa (Babyrousa babyrussa), which we consider low.
Pork consumption, trade, and production are all common in the Philippines (except the far south) and thus the four species of endemic pigs, the Palawan bearded pig (Sus ahoenobarbus), Visayan warty pig (Sus cebifrons), Philippine warty pig (Sus philippensis), Mindoro warty pig (Sus oliveri), are all at high or very high risk (Table 1). In particular, in the central Philippines, there is the critically endangered Visayan warty pig, which survives on only two small islands, and the vulnerable Mindoro warty pig, which is only found on a single island (Linkie et al., 2017).

4.2
Dealing with uncertainty ASF presents immense conservation threats to wild pig species in Asia but the lack of direct research findings inhibits definitive claims. There are two ways to view this uncertainty. The first is to wait until there is sufficient data before raising concern about ASF and mobilizing research and management resources. The second option is to apply the precautionary principle and highlight the potential for serious conservation problems based on the fundamental principles in biology, previous ASF outbreaks, and the currently available evidence described here. We caution that delays in the proactive management of ASF in these regions will have dire ramifications for these threatened species.

CASCADING IMPACTS ON PREDATORS, PLANTS, AND PEOPLE
The spread of ASF to native free-living wild boars poses a threat to populations of large carnivores and human livelihoods. Wild boar is a principal prey species for the endemic and critically endangered Sumatran tiger (Panthera tigris sumatrae) and Javan leopard (Panthera pardus melas) in Indonesia, the Siberian tiger (Panthera tigris altaica), and Amur leopard (Panthera pardus orientalis) in China and Russia (Ripple et al., 2014). The decline of principal prey species threatens dwindling carnivore populations or may shift wild carnivore diets toward forestedge livestock, which has been shown to increase humanwildlife conflict (Braczkowski et al., 2018;Lubis et al., 2020).
If ASF reduces Asian pig populations, there would also be significant cascading impacts on terrestrial habitat structure and plant communities. Asian pig species act as ecosystem engineers through their behaviors of soil rooting, wallowing, seed predation, and nest building (Ickes, Paciorek, & Thomas, 2005). In particular, in unhunted areas, bearded pigs have been shown to be the dominant force shaping tree seedling recruitment (Curran & Webb, 2000;Harrison et al., 2013). On the contrary, in Sumatra and Peninsular Malaysia, Sus scrofa is unnaturally abundant due to crop raiding (Luskin et al., 2014), as are crop-raiding bearded pigs on Borneo (Love et al., 2018), and the cascading impacts of abundant pigs can reduce tree recruitment by up to 62% in the region (Luskin et al., 2017).
A final predicted critical impact of ASF is on the region's people. Locally raised domestic pigs represent a vital food for > 100 million people in the Philippines, Timor-Leste, and parts of Indonesia (BPS, 2010; RPNSO, 2014; Figure 1). In North Sumatra, there were protests against the culling of domestic pigs to control ASF because it would affect local livelihoods. Indeed, a modeling study suggests ASF has significantly reduced incomes, calorie intake, and protein for people in Asia (Mason-D'Croz et al., 2020). Hunting of bearded pigs play a particularly important role for many of Borneo's non-Muslim communities' diet and culture (Bennett, Nyaoi, & Sompud, 2000;Kurz et al., 2020). However, there is little other guidance on wild pigs importance to human diets and culture in other places. Therefore, ASF undermines livelihoods and food security in the region, mainly through lost domestic pork, and could indirectly lead to increased hunting pressure on wildlife species (Pattiselanno & Koibur, 2018).

RECOMMENDATIONS
The current ASF outbreak highlights the lack of measures in place to contain and then curtail its spread. To better prepare for future outbreaks, we make the following key management recommendations:

Carcass and waste disposal
ASF is transmitted via wild and domestic pigs encountering or scavenging carcasses of pigs that died of ASF, or scavenging infected pork products (FAO, 2020). This can be ameliorated with proper destruction and disposal of infected carcasses, such as incineration or sealing carcasses in plastic bags and burying them deep enough to avoid boars or other animals digging them up (European Commission, 2020). Food waste should also be disposed carefully to prevent wild or domestic pigs from accessing infected pork products. We urge governments and conservation groups to devote resources to educating and addressing these issues, especially in rural areas where wild boars can access discarded domestic pig carcasses and trash (Strait Times, 2020).

Surveillance capacity
We advocate increasing testing capacity and implementing diagnostic sampling of all suspicious deaths of domestic, feral, and wild pigs as an early detection system to protect the wild populations of six threatened warty pig species, two bearded pig species, and the three babirusa species on Southeast Asian islands. This must be paired with an open-access online monitoring and reporting system, such as is already being implemented in Europe (The European Food Safety Authority, 2020). Disease surveillance in wild pigs will also aid in the management of ASF in domestic pigs.

Biosecurity measures
For both carcass disposal (#1) and testing infected animals and products (#2), it is critical to implement strict biosecurity measures to prevent the accidental spread of ASF by those in close contact with the disease. This should involve segregation of duty to ensure that veterinary staff or facilities handling contaminated pigs and products are not also connected to farms or wild pig captive breeding centers. Finally, to facilitate contact tracing, we suggest new protocols for recording and sharing information about the trade in domestic pigs, pork, and pork products.

Research
A key knowledge gap is how ASF affects different wild pig species in Asia and we propose urgent investments into research on disease transmission, as well as increased research into assessing and updating the conservation status of these species, for which many lack reliable population data or rely on outdated data (Linkie et al., 2017). Second, the presence of a vector can dramatically change the ecology of the virus, and there is little known about ASF vectors in Southeast Asia. Third, an important limitation for assessing the risk of ASF circulation in Asian wild pigs is the limited information on density estimates for any pig species. There is a need basic ecological studies on pigs and other common hosts of zoonotic diseases.

Public outreach
Management of ASF may also be complicated by people's dependence on pork; for example, in the Indonesian province of North Sumatra, thousands of people from the pork industry, including farmers and restaurant owners, took to the streets to protest against the government's recommended culls (Strait Times, 2020). Thus, clear effective communication about tradeoffs, threats, and policies is also important.

Capacity building
Tracking the spread of ASF in Asia is hindered by expensive disease transmission work that requires laboratories with biosecurity clearance. It may be strategic for local wildlife epidemiologists to coordinate with the additional people and resources being devoted for addressing COVID-19 and other emerging diseases in Asia and globally. Diseases are also blind to borders. Given the looming economic threat ASF poses for developed countries with large pork industries, such as the United States, we suggest they invest in aggressively tackling the disease before it reaches their shores. This would entail partnerships to build capacity in the Southeast Asian countries that are currently on the front lines of the disease. Such efforts could dovetail with initiatives for new wildlife epidemiology research to proactively identify risks for human pandemics and for food systems (Aiyar & Pingali, 2020).

Intersectoral collaborations
Developing relationships between researchers, governments, and local communities that promotes trust, reciprocity, and free flow of data will be central to zoonotic disease detection and control. There are already organizations well positioned to facilitate these collaborations for ASF, such as the One Health initiative (Gibbs, 2014). Further, detection and mitigation activities should be integrated between wild and domestic pigs. An important challenge is therefore promoting intersectoral collaborations between forestry and agricultural departments to address ASF.

CONCLUSION
There is a non-zero chance that ASF could cause multiple mammal extinctions in the near future and this represents an unacceptable tail-risk within conservation biology. Even in more conservative scenarios, such as if ASF remains confined to domestic and free-living Sus scrofa, the epidemic constitutes a serious threat to endangered carnivores, forest plant ecology, and human food security throughout Southeast Asia. Current shortfalls in the response to ASF include insufficient testing to understand transmission and mortality rates, delayed interventions in containing the virus due to economic concerns and politics, and underestimating cascading impacts on livelihoods. We strongly urge developed countries whose pork industries are threatened by ASF to invest in understanding and controlling the disease in the Asia, which will also help mitigate the future impacts of ASF on threatened wild pig species. Otherwise, ASF may limit the ability of affected countries to meet their Sustainable Development Goals of ending hunger and conserving biodiversity.

A C K N O W L E D G M E N T
We thank George Wittemyer and two anonymous reviewers for helpful comments on this manuscript.

A U T H O R C O N T R I B U T I O N S
MSL, ML, and EM wrote the manuscript. S and SS compiled the data and made the maps. All authors contributed to the final version.

ETHICS STATEMENT
The research fell outside of the ethics requirements at our institutions.

DATA ACCESSIBILITY STATEMENT
There is no data associated with this manuscript.

C O N F L I C T O F I N T E R E S T
There are no conflicts of interest.