Opportunities for Transdisciplinary Science to Mitigate Biosecurity Risks From the Intersectionality of Illegal Wildlife Trade With Emerging Zoonotic Pathogens

Introduction

The contemporary scope and scale of the illegal wildlife trade (IWT) is unprecedented (Goldenberg et al., 2017; UNODC, 2020). This transnational environmental crime includes harms against tens of thousands of vertebrates (Scheffers et al., 2019) generating an estimated $5–$23 billion annually (May, 2017). IWT threatens species, ecosystems and societies both locally and globally (Hinsley et al., 2017; May, 2017). IWT is linked to the spread of zoonotic diseases (Gómez and Aguirre, 2008; Pavlin et al., 2009) and is associated with kleptocracy, corruption, money laundering, degradation of the rule of law, national insecurity, undercutting of sustainable development investments, erosion of cultural resources, and convergence with other serious crimes (Shelley, 2018). IWT-related risks are reinforced by the cross-border and transboundary nature of wildlife crime, diversity of wildlife populations, community-based management regimes, and rural-urban connectivity (Hübschle, 2017; Gore et al., 2019). Efforts to reduce risks associated with IWT may generate new risks. For example, indigenous peoples and local communities (IPLCs) have long been seen as either culprits of biodiversity decline or as “unseen sentinels” effectively managing and monitoring their territories. A binary approach to IWT solutions can exclude IPLC cultural and livelihood dimensions of risk management, provoke existing or new environmental injustices. It may also preclude informed consent of people who will be directly affected by decision making (Matias et al., 2020).

Transdisciplinary science can support efforts to promote sustainable and equitable trade of wildlife because IWT involves both overt and covert human behaviors. These behaviors create new biosecurity risks, including spaces, exposure pathways, and transmission routes for emerging and resurgent pathogens. Humans across all stages of the IWT supply chain—from IPLCs to law enforcement officials to conservation biologists—are at risk from exposure to trafficked wildlife and their pathogens, regardless of their intention in interacting with wildlife (Van Borm et al., 2005; Gómez and Aguirre, 2008). Despite the overall human health risks associated with exposure to pathogens with pandemic potential, the connections of IWT with zoonotic pathogens and vector spread, the intersectionality of the issue has not received sufficient attention from the scientific community (UNODC, 2020; WWF Global Science, 2020). Widespread infections and epidemics are potential outcomes of the trafficked wildlife and as seen most recently with COVID-19, a disproportionate risk from pandemics falls on already vulnerable human populations.

A serious problem confronts policy makers who seek to support evidenced based decisions because the intersectionality can create new, significant, or modified biosecurity and environmental risks that remain unquantified. Failing to understand the impact in unmodeled, unmanaged, and unmitigated human health risks can have serious impacts as illustrated by the following discussion of the biosecurity risks associated with pathogens of pandemic potential and IWT. Conversely, opportunities abound to leverage collaborative research and innovative analytic approaches to expand our understanding of IWT and manage future risks in an equitable and sustainable manner (Aguirre and Nichols, 2020). After our discussions of the risks, we consider the biosecurity risks associated with pathogens of pandemic potential and IWT by identifying four scientific opportunities for the use of transdisciplinary science to mitigate biosecurity risks associated with pathogens of pandemic potential and IWT.

Past as Prologue and the Repeating Biosecurity Risks of Zoonotic Transmission

Destruction of habitats in many parts of the world have promoted contact with new species and their pathogens. Furthermore, urban demand for wildlife in particular, illustrated by the size and number of wet markets and wildmeat consumption, often of endangered or threatened wildlife species, are not only hastening species extinction but are changing human-wildlife interactions in ways not previously seen.

Several “stuttering” events occurred over decades since the 1920s before HIV crossed over to humans and was first detected in the 1980s. Wildmeat hunting and subsequent consumption of these catches is thought to be the primary human-wildlife interaction that enabled the spillover of AIDS from chimpanzees to humans (Wolfe et al., 2007; Ordaz-Nemeth et al., 2017). Today, interactions across species are influenced by the rise of the internet and social media that facilitate illicit trade and poaching of endangered and other species across the globe.

In Africa this has been even visually documented. The open and dark web, social media, smart phones and mobile banking enable IWT as ever before (IFAW, 2012; Lavorgna, 2014). Virtual platforms for buying and selling products blur the lines between the legal and illegal wildlife trade, and the lack of monitoring and regulation of virtual “ecosystems” complicate efforts to reduce biosafety risks and promote sustainable trade. The ability to engage in IWT anonymously has increased access to wildlife for diverse stakeholders while at the same time obfuscating some options for pandemic-related contact tracing (Siriwat and Nijman, 2018; FATF, 2020).

Human-wildlife interactions enable zoonotic infections in at least two ways. First, infections can move from animals to humans. This infection pathway is most common in geographies where wet markets, wildmeat hunting, and trade of non-native species are common. This trade is driven by legitimate and illegitimate motivations. These interactions increase the spatial and temporal likelihood of transmission. Second, infections may transfer from humans to other animal species through a process known as zooanthroponosis (Messenger et al., 2014). This less common pathway of transmission can still generate substantial risks. For example, SARS-CoV-2 has been reported in domestic dogs, domestic cats, tigers, and lions (Gönültas et al., 2020; Wang et al., 2020). Spillover of SARS-CoV-2 from humans to mink was also reported in several countries confirmed through contact tracing. As a result, millions of minks have been culled globally (Kevany, 2020; Koopmans, 2020).

Several epidemics and pandemics devastating to humans were detected in recent times including H1N1 swine flu (1.4B infected; 151-575k dead), Ebola virus of 2014-16 in West Africa (28.6 k cases and 11.3 k deaths). Zika virus, SARS and MERS emerged in between these others. These emerging infectious diseases (EIDs) underscore the intersectionality of environmental and animal well-being with maintenance of human health. These outbreaks not only caused the death of hundreds to thousands of people, they increased risks from comorbidity factors such as diabetes, negatively impacted economies, and caused tensions among decision-makers (Madhav et al., 2017; Khubchandani et al., 2020).

The large number of initial patients of COVID-19 associated with a wet market in Wuhan, China originally suggested that the locale, where people closely interacted with legally (and potentially illegally) traded wildlife, was key in its transmission among humans. Some scientists have speculated that the market could, however, have been a focus of human-to-human rather than animal-to-human spread (Mackenzie and Smith, 2020). However, SARS-CoV-2 was not detected in Sunda pangolins (Manis javanica) confirming that this may have been an incidental host in the transmission (Lee et al., 2020). Zoonotic transmission of COVID-19 has not been determined, and ultimately, scientists may never be able to determine a specific animal host and whether it was linked to legally or illegally traded wildlife (Dhama et al., 2020).

A One Health Approach to Surveillance, Biosafety, and Security

Existing collaborations among medical personnel and veterinarians seldom consider the role of IWT in zoonotic transmission of pathogens in surveillance, biosafety, and security (SB&S) efforts (Graham et al., 2013). This observation is striking within the context of One Health (OH), or “the collaborative effort of multiple disciplines—working locally, nationally, and globally—to attain optimal health for people, animals and our environment” (American Veterinary Medical Association, 2008). A OH approach is well-suited for globally distributed challenges such as IWT and pandemics. OH can accommodate dynamic changes in the relationship among humans, wildlife, and ecosystems.

Although academia has moved toward more transdisciplinary research, many challenges remain in governments where agencies tasked with different mandates discourage strong collaborations. A legislation framework will be required to deal with the restrictive nature and slow response to dynamic changes in the landscape (Hyatt et al., 2015). Despite these challenges, integrating theories, methods, and analytical techniques from diverse disciplines with different skill sets can serve as a force multiplier for the policy-relevance of science focused on the threats to human security and global health posed by pathogens of pandemic potential. Pandemic-related impacts such as those associated with COVD-19 (e.g., human death and illness, economic declines, politicization of science) and the increasing sophistication, impact, and economic value of IWT combine to demonstrate that future collaborations and more diverse partnerships are needed. Incorporating OH approaches may be most effective at advancing sustainable and equitable objectives if they engage diverse experts across domains such as conservation criminology, transnational crime, and corruption, supply chain analytics, operations research, and data science. Such transdisciplinary science can at least help clarify a common vision for sustainable use, establish shared values and goals, prioritize equitable allocation of limited resources, guide response protocols, support scalability of decision-making tools, and enhance communication.

We propose four collaborative initiatives to help extend and enhance SB&S efforts in support of more sustainable and equitable treatment of IWT. The OH framework accommodates the range of transdisciplinary perspectives involved in assessing existing SB&S efforts and detection networks for zoonotic pathogens that pose disease burdens for humans and animals. Beyond leveraging existing capacity, technology, and health systems identified through an OH assessment, bespoke, cutting-edge, and locally-sensitive decision and location science-based surveillance and response models can be incorporated to support more effective policy-making and sustainable use of wildlife (Hyatt et al., 2015; Aguirre et al., 2019; Wilcox et al., 2019).

Opportunities to Mitigate Biosecurity Risks Using Transdisciplinary Science

One pathway for improving detection of pathogens in trafficked wildlife is through enhanced technical capacity for effective detection networks, outbreak analysis, and surveillance. Such capacity can generate inferences and inform efforts to decrease the risk of transmission of these pathogens to people and animals. Endemic and cross-boundary zoonotic pathogens (e.g., anthrax, bovine tuberculosis, brucellosis, echinococcosis, Lyme disease) are often underreported or are reported late, due to a lack of local diagnostic capacity and missing data on disease prevalence (Halliday et al., 2012; Tambo et al., 2014). A surveillance system focusing on specific pathogens by country or region along supply chain components of trafficked wildlife requires an understanding of the factors promoting emergence. Identifying approaches for prevention, rapid control, and mitigation is key (https://www.unodc.org/documents/Advocacy-Section/Wildlife_trafficking_COVID_19_GPWLFC_public.pdf). The health, societal, economic, and geopolitical impacts caused directly and indirectly by the COVID-19 pandemic, illustrate the range of risks associated with leaders or public officials who are unable (or unwilling) to identify and respond promptly and adequately to emerging zoonotic pathogens.

Populating a data landscape with analytically relevant variables will enable tracking of trends over time, facilitate aggregation, and disaggregation of data, support monitoring and evaluation efforts, enhance transparency in decision making, and promote accountability to donors. At present, the data landscape is devoid of many of these characteristics, to the detriment of sustainable wildlife use and human health and well-being. We propose actionable opportunities to address these shortcomings.

First, decision makers, civil society, and partner sectors may leverage enhanced SB&S to respond in an appropriate and timely manner to EIDs and strengthen national and local response capacities to prevent future outbreaks. A range of relevant activities includes:

• Comprehensive and co-created prevention education component for at-risk populations.

• A surveillance sample management system for enhanced diagnostic efficiency in collaboration with local partners to further establish or link existing surveillance networks (e.g., Rhinoceros DNA Index System in South Africa https://erhodis.org/).

• Integration of systems analysis and decision science methods within an economic, environmental, social ecosystem and IPLC perspective.

• Integrate transport industry such as aviation providers into enforcement efforts to prevent zoonotic transmission and wildlife trade (USAID, 2020).

• Consideration of the spatiality and intersectionality of wildlife trafficking and biosafety from cross-boundary zoonotic transmission.

Many stakeholders around the world already have the ability to create and manage highly efficient systems and networks across domain areas including logistics, commerce, and health care. SB&S can use those same tools to weaken illicit networks having negative outcomes including health risks, corruption, or abuse (Wood, 1993; Guo et al., 2016). That said, these methods require not only data regarding the nature of disease risk, but also need information on the behaviors of people who participate in those networks that lead to pathogen spillover (Alexander and McNutt, 2010). This requires multi-cultural perspectives and sensitivities.

Second, there exists an opportunity to leverage insights from IPLCs using community-based participatory methods and combining such knowledge with expert assessments, inducing the development of novel analytical tools and approaches that decision-makers can use to respectfully and equitably support local livelihoods by addressing the following enduring challenges: monitoring, detection, prevention, interdiction, and remediation. Improved decision-making for these challenges can be achieved with insights from IPLCs, through a clearer understanding about the operational environment and the economic and societal drivers that motivate local community members to participate in IWT.

Third, decision support models informing behavioral change policies can dramatically enhance local capacity to prevent, detect, and respond to pathogen risks. Supporting compliance with existing rules and enhancing crime analysis and prevention capacity of law enforcement authorities can help address the needs of community members who may otherwise resort to participation in IWT. Participatory methods can help ensure that local populations inform the development of solutions and these strategies are more likely to be consistent with cultural needs and priorities.

At the same time decision-support tools also need to be based on broad systematic evidence appropriate for long term sustainability—and it is imperative that these tools provide ease-of-use and interpretability for implementation by local stakeholders unfamiliar with sophisticated models and diagnostic tools; for example, the common use of Nobuto filter-paper blood samples collected during field surveys to detect exposure to an array of infectious diseases including avian influenza, canine distemper, malaria, and sylvatic plague (Advantec, 2009). Community outreach and engagement can produce accurate and reliable information about the prevalence of wildlife trafficking and EIDs that would otherwise not be known; community engagement will support the sustainability of detection and prevention strategies. We know that poverty, deforestation, urbanization, and human behavior are comorbidity factors underlying EID emergence that may progress into a pandemic (Patz et al., 2004; Aguirre and Tabor, 2009; Hassell et al., 2017). These variables influence epidemiology of pandemics in dynamic ways. Even without the benefit of hindsight on the pandemic, past responses to pandemics reveals that local capacity building, integrative research and transdisciplinary collaborations using the social ecological systems and resilience approach (Wilcox et al., 2019) will be prerequisites to untangle these complex issues that may result in severe harm across large populations. Broader efforts can and should be integrated with our understanding of the illicit wildlife trade. Best practices from efforts to combat other elements of the illicit economy such as study of supply chains, corruption, and illicit financial flows is crucial (Aguirre et al., 2020; FATF, 2020).

Finally, more can be done to harmonize a “network of networks”—including local communities—with enhanced capacity to promote joint SB&S efforts that encourage improved human and animal health, timely reporting, emerging disease detection, and outbreak response along with reporting on IWT. We already have global structures in place to support such a network of networks through science diplomacy, such as The One Health Tripartite Agreement between the Food and Agricultural Organization, World Health Organization and World Organization for Animal Health, supported by the World Bank Group (Vandersmissen and Welburn, 2014).

We can promote resilience in ecosystem function by enhancing education for justice, promoting legislative science advice, and funding interdisciplinary research teams. Science teams can help increase awareness and data integration capacity to facilitate new threat information that can be used strategically and tactically in both responsive and proactive ways. Such information could be particularly useful when it intentionally captures local community knowledge and integrates datasets to dramatically decrease the biosafety security gap between urban and rural areas (OECD, 2020).

Prevention Outweighs Reactive Approaches

Future efforts for containing zoonotic disease of pandemic potential may require a significant shift from scientific prediction to prevention, interdiction, and remediation strategies to deliver any practically beneficial outcomes (Dobson et al., 2020). It also requires efforts to reduce habitat destruction. The COVID-19 pandemic demonstrates that finding a virus, and managing the virus from a public health perspective, are two very different things. The world population and its many different cultures constitutes a complex system within which the virus circulates. Across the social, biological, and engineering sciences there is knowledge, and there are methods that can individually be brought to bear to more fully understand this complex system. More importantly, when diverse disciplines and their resources are brought together to address a complex challenge, they can answer questions and gain insights that no single discipline could generate in isolation.

Conclusions

Supporting SB&S efforts by government agencies and authorities [i.e., 1972 Biological Weapons Convention, 2004 UN Security Council Resolution 1540, 2005 World Health Organization International Health Regulations, Biosafety Level 4 containment laboratories (BSL-4)] from the local to the international levels, is critical for sustainable use of wildlife. These SB&S efforts can create new—and enhance existing—collaborations and capacity to address security issues at the intersection of human and animal health, wildlife trafficking, and infectious pathogens. This intersectionality is well-situated within the OH approach, particularly within the context of current consumption rates of animals for food, culture, traditional medicine, or the exotic pet trade. These activities have persisted for millennia and are highly likely to persist in a post-COVID-19 world. If there are wildlife consumption or trade bans instituted in countries where wildlife products are consumed, what will the impact of these be on curbing disease transmission? How successful would a ban of limited scope be in reducing the risks to human health and well-being from zoonotic transmission? In reality, banning wet markets is unlikely to wholly eliminate or even significantly reduce the disease transmission risks associated with IWT. It may, for example, help drive IWT underground, decrease nutritional options for vulnerable populations, degrade social and cultural identity or alter expressions of power and status. These are phenomena with policy implications that can be most accurately addressed by transdisciplinary scientific research with policy analysis (Alves and Rosa, 2007; Aguirre et al., 2019). Attention can be focused on the supply chains that allow zoonotic pathogens to be so rapidly distributed around the globe. Local capacity building is an essential element of global prevention, and such capacity can be combined with resourceful and well-trained networks at the global level to encourage diverse approaches to sustain biodiversity. This requires unprecedented cooperation by those in the OH world with the specialists in illicit trade in wildlife and illicit supply chains. This also requires transdisciplinary teams spanning science and engineering, environmental studies and social science as well as NGOs and corporations.

We need to ensure that businesses are not complicit in shipping animals with harmful diseases around the world. This requires closer cooperation with the business community such as occurred with the Routes partnership (USAID, 2020). We need interdisciplinary research to address illicit supply chains. More work is needed with the tech sector to ensure that online platforms and social media are not facilitators of illicit sales of endangered species of poached animals, and illicitly obtained flora and fauna. By involving participants at all levels and in all sectors of society we can encourage policies that improve environmental conditions in local communities and at the regional level. Habitat conservation, wildlife protection and a focus on the diverse skill sets of communities is key to accomplishing these objectives. By integrating more diverse scientific disciplines, and their respective scientists with indigenous people and local community insight and risk assessment data, we can promote a more sustainable and equitable wildlife trade.

Data Availability Statement

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding authors.

Author Contributions

All the authors participated in the drafting the manuscript and discussion of all topics related to this perspective manuscript.

Disclaimer

The views expressed in this article are those of the authors and do not necessarily reflect the views of their professional or personal affiliations.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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