Wildlife trafficking: not such a far-flung event

Word count: 18377

Seline Bregman Student number: 01403058

Supervisor: Dr. Jella Wauters Supervisor: Dr. Sofie Ruysschaert

A dissertation submitted to Ghent University in partial fulfilment of the requirements for the degree of Master of Veterinary Medicine.

Academic year: 2019 - 2020

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Preamble This master dissertation was written during the COVID-19 pandemic. The small survey was held before the reached Belgium, so there was no negative effect of the lockdown on this part of the thesis. Moreover, the virus gave an extra dimension to the part about disease emergence linked to wildlife trafficking.

Content Preamble List of abbreviations ...... 1 Summary ...... 2 Introduction ...... 3 1 Illegal wildlife trade in Belgium ...... 5 1.1 Legislation for wildlife trade ...... 5 1.2 Enforcement of the CITES implementation: a small survey in Belgium ...... 6 2 Impact of illegal wildlife trade ...... 9 2.1 Impact on biodiversity ...... 9 2.2 Impact on human society ...... 11 2.3 Health impact on illegally traded animals ...... 12 3 Illegal wildlife trade as a contributor of disease spread ...... 14 3.1 Emergence of disease ...... 14 3.2 Overview of pathogens ...... 16 3.3 Threats to public health ...... 17 3.3.1 SARS-related ...... 17 3.3.2 Human Immunodeficiency Virus ...... 20 3.3.3 ...... 21 3.3.4 Zoonotic risks documented in Belgium so far ...... 21 3.4 Threats to animal health ...... 22 3.4.1 ...... 22 3.4.2 Bovine tuberculosis ...... 23 3.4.3 Chytridiomycosis...... 23 3.4.4 Animal health risks documented in Belgium so far ...... 24 Discussion ...... 25 References ...... 29 Appendix ...... 34

List of abbreviations - ANB – Agentschap voor Natuur en Bos - CBD – Convention on Biological Diversity - CITES – Convention on International Trade in Endangered Species of Wild Fauna and Flora - CR – critically endangered category in the IUCN Red List - CSSE – Centre for System Science and Engineering - DG - Directorate General - EID – Emerging Infectious Disease - EN – endangered category in the IUCN Red List - EU – European Union - EU-TWIX – European Union Trade in Wildlife Information eXchange - FASFC – Federal Agency for the Safety of the Food Chain - GISAID – Global Initiative on Sharing All Data - HIV – Human Immunodeficiency Virus - HTLV – Human T-Lymphotropic Virus - HxNx – used to describe different subtypes of Influenza A . It represents the two main surface antigens: hemagglutinin with 15 subtypes and neuraminidase with 9 subtypes. - IPBES – Intergovernmental Platform on Biodiversity and Ecosystem Services - IWT – illegal wildlife trade - IUCN – the International Union for Conservation of Nature - MERS – Middle East respiratory virus - NGO – non-governmental organisation - NHP – non-human primate - OIE – World Organisation for Animal Health - SARS – severe acute respiratory syndrome - SIV – Simian Immunodeficiency Virus. - SIVcpz – chimpanzee SIV viruses - SIVsm – sooty mangabeys SIV viruses - STLV – Simian T-Lymphotropic Virus - USA – United States of America - VU – vulnerable category in the IUCN Red List - WAHIS – World Animal Health Information System - WHO – World Health Organisation

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Summary Illegal wildlife trafficking, also called illegal wildlife trade (IWT), is of global concern, as it is one of the largest and most profitable organised criminal activities, similar to trafficking in drugs, arms and people. Europe, and thus Belgium, must be considered as an important destination, transit and source region for illegal wildlife. These illegal activities are not a far-flung event in Belgium. The latter is supported in this master dissertation by information collected in interviews e.g. with the Belgium Group Anti-Drugs team at Brussels Airport.

Most legislation and conservation policies are mainly focussed on the effect of IWT on the biodiversity of wild animals. The illegal trade in wild animals is indeed one of the main reasons of the current rapid biodiversity loss, by some called ‘the Sixth Extinction’. However, literature shows that also other important aspects should be considered as potential threats. Corruption, violence, child labour and emerging zoonoses connected to IWT threaten the human population, with the current pandemic of COVID-19 being an obvious and trending example. Literature illustrates the strong connection of IWT with emerging pathogens, transmissible to humans or other animals and thus, being a threat to the public and animal health in Belgium. Thanks to globalisation and international trade, diseases can spread easily and fast.

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De illegale handel in wilde dieren is één van de grootste en meest lucratieve georganiseerde criminele activiteiten ter wereld, ter vergelijken met de handel in verboden middelen, wapens en mensen. Europa, en dus ook België, moet gezien worden als een belangrijke import, transit en export regio voor illegale wilde dieren. Deze illegale activiteiten zijn dus geen ver-van-mijn-bed-show in België, wat toegelicht wordt met verschillende voorbeelden verkregen via het Belgische Group Anti-Drugs team, dat actief is op Brussels Airport.

De meeste wet- en regelgeving is gefocust op het effect van deze illegale handel op de biodiversiteit van wilde dieren. De illegale handel in wilde dieren is inderdaad één van de redenen van de huidige biodiversiteitscrisis, wat door sommigen ‘de Zesde Massa-extinctie’ genoemd wordt. Daarentegen toont onderzoek aan dat er veel andere belangrijke aspecten in acht genomen dienen te worden als potentiële dreigingen. Corruptie, geweld, kinderarbeid en opkomende zoönosen zijn verbonden met de wilde dierenhandel en bedreigen de mensheid, met de huidige COVID-19 pandemie als duidelijk en actueel voorbeeld. In de literatuur worden nog een groot aantal andere pathogenen beschreven die verbonden zijn met deze handel en die kunnen overgaan op mensen of andere dieren. Dit vormt een bedreiging voor de volksgezondheid en de dierengezondheid in België. Met de globalisering en internationale handel kunnen ziektes zich tegenwoordig dan ook gemakkelijk en snel verspreiden.

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Introduction The recent global assessment report of the Intergovernmental science-policy Platform on Biodiversity and Ecosystem Services (IPBES), which displays an interdisciplinary view on the decline of biodiversity, paints a worrying future for our planet1. Since the rise of human civilisation 83% of wild mammals have been gone extinct2. Researchers believe the rate of species extinction is between one hundred and one thousand times higher than before the introduction of humanity (Wilson, 2016). Today, the so-called Sixth Extinction is on its way, mostly driven by human activity (Leakey & Lewin, 1995; Wilson, 2016).

One of the reasons of the rapid loss of biodiversity is the illegal wildlife trade (IWT) (Rosen & Smith, 2010; Sollund, 2016). To protect wildlife species, an international agreement, the Convention on International Trade in Endangered Species of Wildlife Fauna and Flora (CITES), was made to regulate trade herein (Zimmerman, 2003; Braet, 2010; Harfoot et al., 2018). Over 5,800 animal species are protected against wildlife trade via this agreement3. They are listed in the three appendices of CITES. The level of protection in those appendices is supposed to be proportional to the risk of extinction.

The global IWT is one of the most lucrative criminal trades, comparable with trafficking of drugs and weapons, regarding the economy and the organized crime involved (Rosen & Smith, 2010; Duffy, 2016; Sollund, 2016). The illegal wildlife trade is estimated to have an annual value between eight and twenty billion euros, but that is probably just the tip of the iceberg (Duffy, 2016; Smith et al., 2017; Ruysschaert, 2018). This is because legal and illegal trade are often intertwined, which makes it easier to launder or to hide illegal wildlife products (Duffy, 2016). For example, illegally traded python skins can be transported together with legally produced skins, or false papers joining those shipments can state that the skins are produced in captivity instead of originated from the wild (Duffy, 2016). Also, the rewards outweigh the risks, because of the lack of enforcement against violators and the small chance of getting caught (Zimmerman, 2003; Sollund, 2016).

Consumer demand of both legal and illegal wildlife trade can be divided in four categories: pets, traditional medicine, animal products (like meat and leather) and collector items (Rosen & Smith, 2010; Feytens, 2015; Duffy, 2016). The belief in the healing powers of certain wildlife products made some species, such as rhinoceros and tigers, highly popular (Sollund, 2016). In current times of blooming globalisation, open borders, and unlimited connections through the Internet, wildlife and related products can easily be purchased (Sollund, 2016; Ruysschaert, 2018).

A 2018 TV documentary gives an example of illegal wild animal products imported and traded in Belgium. Presenter Stijn Vercruysse and, among others, Erik Verheyen (Koninklijk Belgisch Instituut voor Natuurwetenschappen), investigated the risks and the consequences of bushmeat trade in Brussels4. This documentary showed that Belgium is an important destination for bushmeat, which is not without risks. During an undercover mission in Matonge, an African neighbourhood in Brussels, they were able to obtain three pieces of bushmeat within the timeframe of two days. DNA results showed that the meat originated from different kind of animals on the CITES-list, among which two species of monkeys. Both of them were contaminated with monkey pox, which could convert to a biotype that can cause disease in humans. A recent study of Chaber et al. (2019) also discovered a significant amount of bushmeat coming into Belgium via Brussels Airport every month. Therefore, bushmeat consumption is not only a threat for the existence of those animals, but should also be considered as a threat for public health.

1 IPBES, May 6, 2019: Webcast of the Global Assessment: https://www.ipbes.net/webcast-0; last consultation on May 20, 2020. 2 The Guardian, May 21, 2018: “Humans just 0.01% of all life but have distroyed 83% of wild mammals – study”. https://www.theguardian.com/environment/2018/may/21/human-race-just-001-of-all-life-but- has-destroyed-over-80-of-wild-mammals-study; last consultation on April 22, 2019. 3 CITES species, 2017: https://www.cites.org/eng/disc/species.php; first consultation on April 18, 2019. 4 Pano reportage “Aap op het menu”, October 3, 2018: https://www.vrt.be/vrtnu/a-z/pano/2018/pano- s2018a14/; last consultation on March 20, 2020.

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The problem of IWT is thus not only the fact that organised crime is involved, but also that it plays a role in disease spread and biodiversity loss (Zimmerman, 2003; Rosen & Smith, 2010; Brashares et al., 2014). Additionally, the more a species becomes endangered, the greater its market value on the illicit market (Van Uhm, 2012). This causes a vicious circle, which reinforces the demand to put IWT higher on the political agenda for coordinated action.

In Belgium, the priority of the government for IWT is rather low. This is demonstrated by the limited capacity and resources to control wildlife trafficking and the soft penalties (Feytens, 2015). The customs at Brussels airport seized twenty-eight kilograms of bushmeat in 2017, which is thought to be just a very small portion of the actual trade. Nevertheless, in the past four years (2014-2018) only one official police report has been drawn up5. Moreover, the complexity of the Belgium state structure has a negative effect on an efficient approach (Feytens, 2015). From a previous study by the latter author it is pointed out that the division of the jurisdiction between federal and regional level (i.e. Flanders, Wallonia and Brussels- Capital region) is not clear. This way, as one of the respondents in the study said, multiple systems are in place, however working uncoordinated.

It is well-known that globalisation and traffic all over the world, contributes to the spread of certain diseases. West-Nile disease, African horse sickness and , for example, have recently been identified as potential threats for Belgium (Dewulf, 2017). Additionally, legal and illegal wildlife trade is associated with zoonotic risks (Rosen & Smith, 2010). The current SARS-CoV-2 or COVID-19 pandemic is likely caused by a pathogen with a wildlife reservoir, that most likely spilled over to humans at a wildlife market in Wuhan (Zhou et al., 2020). Because the exact extent of IWT is uncertain, the risks involved herein are not fully documented, despite being very relevant. Assessing the risks and prevalence of disease spread by IWT for Belgium, as well as the low survival rate of individuals in a batch of smuggled animals, can contribute to persuading the government to take this issue more serious.

This thesis will analyse wildlife trafficking, and its definition. The current situation in Belgium will be discussed by combining information from literature with results of interviews of two officers of the Group Anti-Drugs team (GAD-team) at Brussels Airport, a CITES-officer of the CITES-unit of Belgium and an inspector of the Agentschap voor Natuur en Bos in Flanders. The initial contact and further discussion were established via telephone calls and email. The officers of the GAD-team were also interviewed in person.

Additionally, the impact of wildlife trafficking on our planet will be highlighted, including the rapid decline of biodiversity with its consequences, and the epidemiological effects such as introduction of zoonotic diseases. An overview of available literature, with emphasis on diseases correlated with IWT, will be summarized and illustrated by graphs, pictures and tables.

5 De Standaard, October 3, 2018: Zaventem draaischijf voor bushmeat. http://www.standaard.be/cnt/dmf20181003_03805093; last consultation October 10, 2018.

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1 Illegal wildlife trade in Belgium Wildlife trafficking, or illegal wildlife trade (IWT), involves the sourcing, selling and consumption of wildlife commodities (Travis et al., 2011). This is of global concern, as it is one of the largest and most profitable organised criminal activities (Zimmerman, 2003). Wildlife includes all non-human animals and plants and their derivates that are in their natural environment (Wyatt, 2013). The focus of this thesis lies on the illegally trafficked animals and their products.

The European Union (EU) is a destination, transit, and source region for trafficking in endangered species6, and Belgium is no exception (CITES Belgium, 2018; Musing et al., 2018). A TRAFFIC report of 2018, presenting a survey of CITES species traded between 2007 and 2016 in Belgium, showed that 1,264 seizures were reported in that period, of which 69% involved species of fauna (Musing et al., 2018). Noteworthy were the 19,370 confiscated seahorses (plus an extra 80 kilograms of dried seahorses), the 3,615 pieces of ivory and the 1,424 leather products made from protected Crocodylia and Serpentes spp. (Musing et al., 2018).

Recently a study on bushmeat impounded at Brussels Airport in 2017/2018 was published (Chaber et al., 2019). Chaber et al. (2019) conducted this research in collaboration with the Belgium customs and the Federal Public Service of Health, Food Chain Safety and Environment (FPS Public Health). It is estimated that an average of 3,653.7 kilograms of bushmeat, which has originated from Sub-Saharan Africa, is brought through Brussels airport every month (Chaber et al., 2019). This brings us to a total of 43,844.4 kilograms of bushmeat per year.

Culture, social aspects, micro-political reasons, taste preferences, nostalgia and homesickness amongst Europeans and people of African origin are just a few examples of factors that can explain the demand for bushmeat in Europe and therefore Belgium (Chaber et al., 2019). The main originating countries are Cameroon, Togo, Ivory Coast and the Democratic Republic of Congo (Chaber et al., 2019). Bushmeat is available for sale in Belgium, for example, in the Brussels neighbourhood Matonge. As mentioned earlier, the researchers for the Belgian program Pano could buy illegal bushmeat in a few different stores7.

1.1 Legislation for wildlife trade The relevant legislation for international wildlife trade can be divided in animal health (same as for livestock trade), animal welfare and the international movement of endangered species (Fèvre et al., 2006). The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) is an international agreement between governments, aimed at protecting wild animals and plants from overharvesting by humans for international trade8. The three appendices of CITES divide the species in order to the threat of extinction, appendices I being the most threatened9. Another important international convention for wildlife conservation is the Convention on Biological Diversity (CBD) (Fèvre et al., 2006). The International Union for Conservation of Nature (IUCN) is an important organisation for wildlife trade, which is an initiative from UNESCO in 1948 (Fèvre et al., 2006). A meeting of members of IUCN in 1963 resulted to draft CITES8.

6 European Commission - Enviroment: The EU Approach to Combat Wildlife Trafficking. Last updated August 7, 2019: https://ec.europa.eu/environment/cites/infographics_en.htm; last consultation on April 17, 2020. 7 Pano reportage “Aap op het menu”, October 3, 2018: https://www.vrt.be/vrtnu/a-z/pano/2018/pano- s2018a14/; last consultation on March 20, 2020. 8 CITES - What is CITES?: https://cites.org/eng/disc/what.php; last consultation on May 19, 2020. 9 CITES - CITES species, 2017: https://www.cites.org/eng/disc/species.php; last consultation on April 18, 2019.

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The EU regulation of CITES (Council Regulation (EC) No 338/97 and Commission Regulation (EC) No 865/2006) is supplemented in the Belgium law of July 28, 198110. This law provides penalties, the designation of supervisory authorities and stricter provisions on certain species. As one of the 183 parties of CITES, Belgium designates a management authority, called the CITES Unit of the Service Multilateral and Strategic Affairs (AMSZ), part of the Directorate General Environment (DG5) of the FPS Public Health11. It is responsible for issuance of permits and certificates, communication to the public, training of the supervisory authorities and (bi)annual reporting to the higher CITES secretariat10.

Supervisory authorities play a crucial role in the enforcement of the implementation of CITES10. Customs, e.g. the Group Anti-Drugs at Brussels airport, are responsible for the controls at the point of entry in Belgium. They work closely together with the inspectors of the Federal Agency for the Safety of the Food Chain (FASFC). The police and the inspection department of the FPS Environment are other important actors of CITES enforcement in Belgium. On regional level, the Agentschap voor Natuur & Bos (ANB) organises nature inspections together with FASFC in the Belgian region Flanders, which comprehend a small piece of the enforcement of CITES regulation as well12. Other regional authorities are the Service Public SPW Agriculture, Ressources Naturelles et Environnement in Wallonia13 and Leefmilieu Brussel in Brussels14. The CITES implementation in Belgium is summarized in Fig. 1.

Management authority •CITES-unit

•Customs (e.g. GAD-team) •FASFC-inspectors •Police Supervisory authorities •FPS Enviroment inspectors •ANB inspectors (Flanders) •SPW Agriculture, Ressources Naturelles et Environnement inspectors (Wallonia) •Leefmillieu Brussel inspectors (Brussels)

Scientific committee

Figure 1 – Organogram of the structure of the CITES implementation in Belgium. Adapted from: FPS Public Health10. 1.2 Enforcement of the CITES implementation: a small survey in Belgium A few officers of the Group Anti Drugs (GAD-team), one actor of the supervisory authorities of CITES in Belgium, were contacted for this study to get a view on illegal wildlife trade in Belgium. These officers are responsible for the luggage controls at Brussels Airport to intercept illegal packages, mainly focussed on illegal drugs. Examples of their seizures of recent years are demonstrated in the figures 2 till 6.

10 Federal Public Service Health, Food Chain Safety and Environment. How does CITES work in Belgium?: https://www.health.belgium.be/en/animals-and-plants/animals/cites-and-endangered- species/how-does-cites-work-belgium; last consultation on April 15, 2020. 11 Federal Public Service Health, Food Chain Safety and Environment. What does CITES do?: https://www.health.belgium.be/en/animals-and-plants/animals/cites-and-endangered-species/what- does-cites-do; last consultation on April 15, 2020. 12 Agentschap Natuur & Bos. Natuurinspectie onderschept grote lading beschermde vogels. Oktober 2, 2019. https://www.natuurenbos.be/pers-nieuws/nieuws/natuurinspectie-onderschept-grote-lading- beschermde-vogels; last consultation April 15, 2020. 13 SPW Agriculture, Ressources Naturelles et Environnement: https://spw.wallonie.be/organigramme- spw-agriculture-ressources-naturelles-et-environnement; last consultation May 19, 2020. 14 Leefmilieu Brussels: https://leefmilieu.brussels/; last consultation May 19, 2020.

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Figure 2 & 3 – Hawk eagles in hand luggage from Bangkok via Vienna. Confiscated and pictures by the GAD-team.

Figure 4, 5 & 6 – Two monkey skulls and unidentified bushmeat, in total 10 kilograms of fresh meat. Confiscated from a direct flight from the Democratic Republic of Congo in 2018. Pictures by the GAD-team. The GAD-team is additionally responsible for checking postal packages coming into Brussels Airport, based on a risk analysis of the origin of the parcels. Regular mail can be used for quick and anonymous transport and it usually involves delivery of an Internet order. In the current “digital age”, wildlife and its products are thus more easily accessible (Harrison et al., 2016; Ruysschaert, 2018). For example, during research of TRAFFIC in 2016 it was found that Malaysians used Facebook for trading several species15, including the Flat-headed cat (Prionailurus planiceps) and the Pig-tailed Macaque (Macaca nemestrina) that are both endangered according to the IUCN-Red List16. An example of living animals seized in mail in Brussels Airport is illustrated in Fig. 7 and 8.

Figure 7 & 8 – Living turtoises in mail to Belgium. Pictures by the GAD-team. The controls executed by the customs are planned according to a risk-analysis, since there is too little capacity to control every item. The highest risk was determined for the Hainan flights from Belgium to China, which normally takes place five times a week. This risk analysis for transfers was pointed as being problematic by one interviewee. If a plane arrives from Africa into Belgium, it would normally be ranked in the “high-risk” category and therefore the luggage will be checked. But if the passenger and his luggage are on transfer to another country, the luggage does not need to go through security and will be brought straight to the next airplane. This plane will arrive in another country where it probably escapes a high-risk ranking and check-up as the plane is categorized as incoming from a “low-risk” European country.

15 TRAFFIC March 3, 2016. Trading Faces: Malaysia the use of Facebook to Trade Wildlife in Peninsular Malaysia. https://www.traffic.org/publications/reports/trading-faces/; last consultation April 16, 2020. 16 IUCN Red List. https://www.iucnredlist.org/; last consultation April 16, 2020.

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For CITES prosecution in the case of bushmeat, identification of the species is required. Meat seized at airports is normally immediately incinerated as required by European legislation (Chaber et al, 2019). Meat from livestock or from protected wildlife are thus treated the same way. A macroscopic differentiation between those two is not always easy and identification by the owner cannot be trusted.

Not only the financial reward for importing illegal wildlife is high (e.g. a rare pair of parrots can be sold for €50,000 in Europe), clearly the penalties if caught are low and rarely enforced (Sollund, 2016; Chaber et al, 2019). This is not only the case in Belgium, the absence of focussed effort due to lacking resources and political support is seen around the world (Wilson-Wilde, 2010; Sollund, 2016). The latter is illustrated by a particular case reported by the GAD-team. A leopard skin (Panthera pardus) and three belts in crocodile leather were found in the checked-in luggage from a Chinese citizen, who came from Kinshasa and went via Brussels Airport to Beijing. He was arrested and handed over to the Federal Police for further investigation but was released after examination to board on another plane. The CITES items were seized and there were no further repercussions.

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2 Impact of illegal wildlife trade 2.1 Impact on biodiversity Conservationists look at wildlife trafficking rather from a point of view of the risk of extinction rather than risk of crime occurrence (Kurland & Pires, 2016). The risk of extinction of animals, plants and fungi is internationally assessed in the IUCN Red List of Threatened Species, established in 196417. Species that are most threatened for their survival are found in the three threatened categories: critically endangered (CR), endangered (EN), and vulnerable (VU)17. This list is often used to revise policies, e.g. via the recent IPBES report18, and important agreements, such as CITES regulations and the Convention on Migratory Species (CMS)19.

As defined by Fa et al. (2009), hunting is “the extraction of any wildlife, from the wild, by whatever means and for whatever purpose”. Currently hunters overexploit many biodiverse areas for an expanding international wildlife trade (Kurpiers et al., 2016). Consumer demand of both legal and illegal wildlife trade can be divided in four categories: pets (especially primates, birds and reptiles), traditional medicine, animal products (like meat and leather) and collector items (Fa et al., 2009; Rosen & Smith, 2010; Duffy, 2016). Due to the increase of human population, the demand and the trade in wildlife has risen dramatically (Fa & Peres, 2001; Bell et al., 2004; Wyatt, 2013).

Easier access to firearms and other advances in hunting practices increased the likeliness of successful hunt and is therefore partly responsible for the current overexploitation of wild animals (Chaber et al., 2019). The overharvesting of animals and plants is one of the reasons for the global disappearance of the most vulnerable species (Fa et al., 2009; Travis et al., 2011; Harfoot et al., 2018). This increase in hunting success can explain the high extraction rates of wildlife species in many Sub-Sahara African and Asian countries (Fa & Peres, 2001; Swift et al., 2007).

The hunting of animals goes along with a few additional problems that drive wildlife species to extinction. First, the highest hunting pressure often lies with high-body mass animals or endemic species (Fa et al., 2009; Ripple et al., 2016), as illustrated in Fig. 9. Moreover, hunters have a preference for adult animals (Chaber et al., 2019). The latter combined with the low reproduction rate of these species is an additional threat to the species’ survival (Kurland & Pires, 2016; Chaber et al., 2019). While reproductively active adults are killed in a wink, it takes time for new-borns to reach the reproductive age (Ripple et al., 2016).

Figure 9 – Terrestrial mammal species threatened by hunting in (a) numbers and (b) percentage, grouped by their body mass in kilograms. From: Ripple et al., 2016.

17 IUCN Red List background and history: https://www.iucnredlist.org/about/background-history; last consultation April 20, 2020. 18 IPBES, May 6, 2019: Webcast of the Global Assessment: https://www.ipbes.net/webcast-0; last consultation on April 20, 2020. 19 IUCN Red List uses: https://www.iucnredlist.org/about/uses; last consultation April 20, 2020.

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Secondly, hunting on wildlife species causes collateral damages. The hunting methods can be destructive – e.g. nesting trees are cut down, neonates are separated from their mother (Sollund, 2016) – but most importantly the ecosystem gets disturbed (Chaber et al., 2019). The extinction of habitat landscapers, such as large-bodied animals, can drive long-term changes in the composition of ecosystems (Fa et al., 2009; Symes et al., 2018). These key species shape the landscape, e.g., by spreading seeds or keeping a balance in the composition of the animal species (Fa et al. 2009; Chaber et al., 2019). An illustrating example is the re-introduction of wolves in the Yellowstone National Park20. The wolves had a cascade of effects that changed the ecosystem and physical geography of the Yellowstone National Park in North America in only 15 years after their reintroduction (Ripply and Beschta, 2012; Dobson, 2014).

In addition, wildlife trade and other major drivers of biodiversity loss seem to work synergistically (Symes et al., 2018). Symes et al. (2018) did their study in Sundaland, a biodiversity hotspot in Southeast Asia that acutely suffers from habitat loss, hunting and wildlife trade, to comprehend the combined effect of deforestation and exploitation of 77 species. They concluded that the combination of habitat loss and wildlife trade amplifies the decline of these species more than three times. This illustrates that we are likely to underestimate the extinction risk of traded species (Symes et al., 2018). Based on their outcomes, the authors suggested to increase the list of species being threatened (CR, EN or VU) with 89% on the IUCN Red list (51 species, compared to 27 species now).

This is not the only study that suggest that the IUCN Red List needs a coordinated update (Rueda- Cediel et al., 2018). Sometimes controversies can be found between the IUCN Red List and the CITES- list as well. For example, the newly discovered African mangabey Rungwecebus kipunji is listed as an endangered species in the IUCN Red List (Davenport, 2019). However, with only 68 square kilometre (scattered) area of occupancy (Davenport, 2019), this animal is still below the range of 100 square kilometre criteria for being labelled as critically endangered (Davenport et al., 2008). Controversially, this animal is listed in Appendix II of the CITES-list (“not necessarily now threatened with extinction but that may become so unless trade is closely controlled”21), while illegal hunting is indeed one of the threats for this species (Davenport, 2019). Notion must be made that these lists, even though not always up to date, are the only comprehensive frame of reference.

The snob-effect is what economics describe as the situation driven by the desire to own rare and expensive goods (Chen, 2015). Research shows that people have a greater demand for rare or endangered species (Wilson-Wilde, 2010; Chen, 2015). Because most targeted species are slowly becoming extinct, they become more rare, and consequently more exclusive for people who are willing to spend large amounts of money on them (Chen, 2015). A study done by Hauenstein et al. (2019) showed a positive correlation between ivory price and annual variation in poaching rates, meaning that poaching rates were higher when the ivory price was increased. Nowadays white rhinoceros’ horn is worth as much as two times their weight in gold22. The compulsive desire for exclusivity makes the fourth additional factor connected to the biodiversity loss related to IWT.

The last factor favouring biodiversity loss is the contribution of IWT to the introduction of invasive species and diseases (Wyatt, 2013). The globalisation, international trade and travel are responsible for the increasing distribution of non-native species around the world (Wyatt, 2013). Invasive species are a human-induced stressor and causes disbalance in the native ecosystem (Sax and Brown, 2000). The hypotheses for the success of these alien species are the absence of their natural enemies, the competitive superiority over native species and the opportunistic use of ecological circumstances in human disturbed environments (Sax and Brown, 2000).

20 Yellowstone National Park: https://www.yellowstonepark.com/things-to-do/wolf-reintroduction- changes-ecosystem; last consultation April 20, 2020. 21 The CITES Appendices. https://www.cites.org/eng/app/index.php; last consultation May 14, 2020. 22 European Commission - Enviroment: The EU Approach to Combat Wildlife Trafficking. Last updated August 7, 2019: https://ec.europa.eu/environment/cites/infographics_en.htm; last consultation on April 17, 2020.

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2.2 Impact on human society Illegal wildlife trade has not only impact on the biodiversity, but also on human society. IWT is among the most profitable forms of organized crime in the world (Kurland & Pires, 2016). Estimations suggest that IWT is worth more than $20 billion per annum (Wilson-Wilde, 2010).

The recurring factor of wildlife hunting is poverty (Van Uhm, 2016; Hauenstein et al., 2019). Poverty is often identified as the cause of illegal wildlife hunting and poaching (Duffy et al., 2016). For example, the headcount ratio of people living under the poverty line ($1.90 per day) in the Sub-Saharan Africa is 41.1%, according to the latest estimation of the World Bank Group in 201523. Literature showed that this is one of the hot spots of illegal bushmeat supply (Fa et al., 2003; Swift et al., 2007). If considering ivory poaching, there is a positive correlation between the site level variation of poaching and the poverty density (Hauenstein et al., 2019). Hauenstein et al. (2019) conclude that reducing poverty and corruption may have a greater effect to reduce elephant poaching, than improving law enforcement.

For African countries, the bushmeat consumption is estimated on one billion kilograms every year (Karesh et al., 2012). In many West and Central African countries, the bushmeat is an important source of animal protein, with up to 90% of meat consumption coming from wild animals (Fa et al., 2003). Household economies at hunting sites and individual households depend for a range of 38% to more than 90% of the total income on bushmeat hunting and trade (Wyatt, 2013; Kurpiers et al., 2016).

Wild meat is often the most accessible and cheapest form of protein source (Fa et al., 2003). The preference for wild meat is due to the low productivity of domestic livestock in tropical forest conditions, and the investment and risks associated with keeping livestock (Fa et al., 2009). Extensive livestock husbandry is rarely feasible in these areas (Fa et al., 2009). Plus, the cost of bushmeat production is lower than the cost of raising livestock (Fa et al., 2009), which is an important factor in developing countries. Besides its connections with poverty and the inability of raising livestock, hunting and consuming bushmeat must also be considered as a part of culture and won’t necessarily stop when poverty ends (Duffy et al., 2016; Chaber et al., 2019).

The growing global demand on wildlife has led to overexploitation of wild animals (Wyatt, 2013; Van Uhm, 2016). This eventually leads to critical loss of resources for people depending on it, and when the sources become scarce, this may eventually lead to inter-human conflict as well (Travis et al., 2011; Wyatt, 2013; Van Uhm, 2016). Because of the decline of the sought-after species, hunters are forced to exploit new areas of wildlife, which in poor countries often relates to cheap child labour to access more difficult terrains (Brashares et al., 2014).

Trade bans and associated seizures are part of the reason of the increased prices of illegal wildlife and its products (Hauenstein et al., 2019). Besides the higher reward for the poacher’s efforts, many examples of illegal markets tell that law enforcement becomes inadequate when commodity prices rise (Hauenstein et al., 2019). This means that the incentives of hunting and trading protected wildlife will increase, responding to the higher reward of illegal wildlife. If the investment in law enforcement and penalties are not increased accordingly, they will stay insufficient.

Additionally, the professional crime network of illegal wildlife is connected to corruption and violence (Wyatt, 2013; Van Uhm, 2016; Wyatt et al., 2018). In some extreme cases, corrupt officers control the law enforcement and the court, allowing the wildlife market to continue and benefitting from it as well (Wyatt, 2013). Sometimes it involves one individual, but as suspected in the case of North Korea, the government itself can also be participant in the IWT (Wyatt, 2013). Another of many examples is the instability of the government in Kenia, resulting in a large increase of illegal trade (Fèvre et al., 2006).

23 World Bank Group – Press release September 19, 2018: Decline of Global Extreme Poverty Continues but Has Slowed: https://www.worldbank.org/en/news/press-release/2018/09/19/decline-of- global-extreme-poverty-continues-but-has-slowed-world-bank; last consultation April 18, 2020.

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At last, IWT also undermines legal trade and has a negative effect on local communities22. This is especially the case for tourism in game reserves. Tourism in countries such as Tanzania and South Africa are largely reliant on wildlife tourism. For example, the tourism in the nature reserve Serengeti in Tanzania generates $500 million per year22. With the decline in biodiversity and loss of iconic species, the tourism reliant economies take a hard hit.

2.3 Health impact on illegally traded animals Wildlife trafficking has also an impact on the health of the traded animals. Captivity and transport of animals can trigger a stress-response with elevated cortisol-levels (Fell and Shutt, 1986; Bayazit, 2009; Heiken et al., 2016). Confiscated animals from IWT were usually transported in high densities, with poor ventilation and inadequate food (Godoy et al., 2010). A good example is the confiscation of the 1,529 living exotic turtles, worth €76,500, by the Bureau of Customs NAIA in Pasay City (the Philippines) on March 3, 201924. These turtles were packed together in four suitcases, with duct tape around them to limit their movement as shown in Fig. 10. Fig. 11 shows illegally trafficked cockatoos packed in empty bottles in Indonesia25, and in chapter 1 other examples are shown in Fig. 2, 3, 7 and 8.

Figure 10 – Turtles packed with ducktape in suitcase24. Figure 11 – Cockatoos packed in empty bottles25. The inappropriate conditions in which these animals are trafficked are largely responsible for the high mortality rate before they reach their destination (Marano et al., 2007). For both birds and reptiles, this can reach up to 90% (Warchol et al., 2003; Sollund, 2016).

Stress, in general, can lead to immunosuppression, which provides a favourable environment for pathogen growth, allowing the surfacing of subclinical diseases (Vitlec et al., 2014; Cain & Cidlowski, 2017). This is especially relevant, since these animals frequently carry pathogens (Karesh et al., 2007). This must be considered as a contributing factor to the health issues of traded animals themselves, and to the spread of emerging infectious diseases (EIDs), including zoonoses, which will be discussed in chapter 3.

Godoy et al. (2010) found that most illegally traded birds in São Paolo died because of infectious processes, most of which were viral. An estimation of 5% of the wild bird population in Brazil are healthy carriers of avian poxvirus (Ritchie, 1995). The disease surfaces due to the immunosuppression caused by the stress of transportation (Godoy et al., 2010). The poxvirus is then spreading easily to the other animals in the same parcel, which was (in this case) lethal for 102 out of 360 birds (Godoy et al., 2010).

24 Facebook post of Bureau of Customs NAIA on March 3, 2019. https://www.facebook.com/pg/bocnaia/posts/?ref=page_internal; last consultation March 19, 2020. 25 Briggs, H., October 7, 2019. Global wildlife trade higher than was thought. BBC News website. https://www.bbc.com/news/science-environment-49904668; last consultation March 19, 2020

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Non-infectious causes can also contribute to the health issues of illegally traded animals. Starvation, dehydration and traumatic injuries are not uncommon and can be responsible for death (Godoy et al., 2010). Both can make the animal more susceptible for infectious diseases as well.

Trafficked animals that survive the transport, enter a completely new environment, with other conditions and unknown endemic pathogens. Often, the animals are not adapted to this new environment and do not have immunity to the new pathogens, which causes stress. As mentioned before, stress leads to favourable conditions for pathogens to thrive and thus for possible additional health issues upon arrival.

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3 Illegal wildlife trade as a contributor of disease spread It is known that transport of humans and animals contributes to the spreading of certain diseases (Fèvre et al., 2006; Travis et al., 2011; Smith et al., 2017). The threat of emerging infectious diseases (EIDs) is increasing since the 1980s (Jones et al., 2008; Pavlin et al., 2009; Karesh et al., 2012). Increasing human encroachment into wild lands, especially disease “hot spots”, is mostly at fault for the increase of EID (Jones et al., 2008). Hundreds of billions of dollars of economic damage globally is caused by the disease outbreaks resulting from wildlife trade (Karesh et al., 2007). One of the currently best illustrating examples is the pandemic of SARS-CoV-2, better known as COVID-19.

Even though the focus of wildlife trade mostly lies at biodiversity loss, the large wildlife trade also poses great threat to public and animal health (Karesh et al., 2005; Fèvre et al., 2006; Smith et al., 2017). Notion must be taken to the uncertain numbers of IWT, which makes a true assessment of the risk difficult (Gomez & Aguirre, 2009; Karesh et al., 2007; Smith et al., 2017). In addition, unofficially traded animals are a much greater risk factor for disease spread, because they are not necessarily subject to veterinary controls (Fèvre et al., 2006; Karesh et al., 2007; Pavlin et al., 2009).

3.1 Emergence of disease The emergence and re-emergence of infectious diseases seem to be mostly driven by human movement and manipulation of domestic and wild animals, including globalized trade (Travis et al., 2011; Smith et al., 2017). The increasingly global scope of IWT and the destruction of wild habitat contribute to the rising threat of the EIDs (Karesh et al., 2007).

The global IWT is a lucrative criminal trade covering an immense network (Rosen & Smith, 2010; Duffy, 2016; Sollund, 2016). There is at least a plurality of one billion (in)direct contacts between wildlife, humans, and domestic animals as a result of wildlife trade annually (Karesh et al., 2005). The expanding trade network of hunters to consumers, with a lot of people along this commodity chain, means that there are many points were disease can be spilled over (Karesh et al., 2007; Kurpiers et al., 2016).

In the past hunters in rural communities went hunting for their own immediate consumption, which meant an increased risk of for themselves, but unlikely a risk of a major outbreak of infectious disease (Swift et al., 2007; Kurpiers et al., 2016; Smith et al., 2017). They remained local and the likelihood of an epidemic was limited, due to generally small tribes which are widely scattered, impeding disease spread between large groups of people (Kurpiers et al., 2016).

The latter is no longer the case as remote rural areas are more connected to urban areas (Kurpiers et al., 2016; Smith et al., 2017). Epidemic potential is greater in urban areas due to the higher concentration of people, and directly also higher concentration of vulnerable people (Swift et al., 2007). This includes people of young and old age, pregnant women and immunodeficient people. The one billion kilograms per year of bushmeat consumption in African countries only is an important transmission way for zoonoses (Karesh et al., 2012). On top of this, there is a shift from local subsistence hunting to the sale of hunted animals into an expanding transnational wildlife trade (Bell et al., 2004).

After the hunt, the animals are often sold at so called ‘wet markets’26 (Karesh et al., 2005). Living animals are stored in cases on top of each other, waiting to be sold as freshly slaughtered meat. These markets have an amplifying effect on the diseases they are carrying due to the body fluids that can spill from one species to another (Karesh et al., 2005). There is extensive cross-exposure between species that normally would not mix or be in contact under natural conditions (Bell et al., 2004; Karesh et al., 2007). This facilitates viral change and host adaptation (Alexander et al., 2018).

26 60 Minutes Australia - Journalist goes undercover at "wet markets", where the started, March 8, 2020, on YouTube. https://www.youtube.com/watch?time_continue=6&v=Y7nZ4mw4mXw&feature=emb_logo; last consultation March 23, 2020.

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Emergence of diseases requires interspecies contact between the natural host of the pathogen and incidental hosts (Wang et al., 2006; Kurpiers et al., 2016). A natural host may be carrier of the disease without showing any symptoms and serve as a reservoir of the pathogen (Kurpiers et al., 2016; Alexander et al., 2018). An incidental host, however, is more likely to be affected by the pathogen and may even transmit it (Kurpiers et al., 2016). Those incidental hosts are shown in Fig. 12 as the intermediary host and the focal host. Spillover and emergence randomly occur, of which the outcome depends on the overcoming of the spillover boundaries (SB1 route for direct transmission; SB2-SB3 route for indirect transmission) and the ability of focal host-to-host transmission (Wang et al., 2006; Alexander et al., 2018). The process of spillover and emergence is illustrated in Fig. 12.

Figure 12 – Model of the process of pathogen spillover and emergence. The reservoir component (RC) is where the pathogen is endemically present; the intermediary host/vector component (IHC) serves as a transfer from the RC to the focal host (FHC); the focal host component (FHC) are incidental host (generally human or other animals of particular concern). The white dotted lines show the spillover boundaries SB1 till SB3 (SB1 route for direct transmission; SB2-SB3 route for indirect transmission) and the red dotted lines show that not every spill over ends in a successful emergence of disease. From: Alexander et al., 2018.

Generalized pathogens have the most potential to become emerged, especially when they can infect more than one taxonomic order (Kurpiers et al., 2016). The spread of the disease is faster if the pathogen can be transmitted by his incidental host and is thus a greater risk for public and animal health (Alexander et al., 2018). Taylor et al. (2001) found that 33% of the zoonotic agents were known to be transmissible between humans and 3% of all zoonoses are considered to have their main reservoir in humans. These numbers may be out-dated at this moment, as the recent outbreaks of SARS- coronaviruses were not taken into account in this study (see chapter 3.3.1).

Microbiological changes or adaptation is also involved in the emergence of certain diseases from wild reservoirs (Kruse et al., 2004). Examples of these changes are mutations, antigenic shift, genetic recombination, and conjugation (Nester et al., 2007), of which two are demonstrated in Fig. 13. The transmission of these changed pathogens from wildlife to humans, either directly or indirectly through domestic animals, can happen in multiple ways like already pinpointed before (Kruse et al., 2004; Kurpiers et al., 2016).

A good example of this finding is the genetic reassortment (Fig. 13B) that can happen when a person is infected with an avian and a human Influenza virus (Kruse et al., 2004). A new subtype of the virus will potentially emerge in a population that is immunologically naive to this type. This antigenic shift could lead to another pandemic of influenza, such as the one in 1918. Another important microbial change in influenza is antigenic drift, which is common in RNA viruses such as SARS-related coronaviruses and Influenza virus (Nester et al., 2007). As a result of this antigenic drift, which includes small mutations of the H and N antigens, the immunity build to the first variant of the virus is no longer effective to the new variant (Nester et al., 2007). Hence, a previously immune person can become infected by, and even sick from, the new variant of the virus.

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Figure 13 – Two examples of microbiological changes that can be involved in the emergence of certain disease from wild reservoirs. A. Simple model for recombination of two virus strains with linear non-segmented genomes. Recombination may occur when a viral polymerase is replicating the two strains in a co-infected host cell. B. Simple model of re-assortment in RNA virus with a segmented genome. Each segment of the genome can be exchanged when two variants are in co-infected host cell. The reassortant virion is formed with a different strain, with segments donated by both ‘parents’. In case of Influenza virus, it means that a new combination of H and N antigens can be assorted. From: Lam et al., 2010. The overexploitation of the areas where once the highest level of biodiversity was found, has not only drastic effect on the biodiversity but does also mean that hunters need to exploit new source populations (Bell et al., 2004). They will thus have direct contact with other kinds of animals and their potential unknown pathogens.

Other human behaviour also has his impact to the increase of EID. Camping, hiking and (trophy) hunting are activities that may present risk factors for certain zoonoses, like tickborne diseases (Kruse et al., 2004; Karesh et al., 2012). With over a billion international travellers every year, infected people can aid the spread of zoonotic diseases anywhere in the world (Karesh et al., 2012).

Also, the increasing livestock production in developing countries without important disease controlling measures might lead to the emergence of other pathogens (Karesh et al., 2012). Because these diseases have a reservoir in wild animals, there is a continuous risk of emergences. Such diseases may thus consequently never be completely eradicated by vaccination, in contrast to diseases that only have a human reservoir e.g. (Nester et al., 2007).

The globalisation and modern transportation increase the risk of worldwide spreads and emergence of these diseases (Kruse et al., 2004; Karesh et al., 2007; Marano et al., 2007; Brashares et al., 2014). The movement over vast distances through an expanding wildlife trade network is contributing to the favourable conditions for disease spread (Bell et al., 2004). The Internet must also be considered as a facilitating factor, since it significantly promotes access to (illegally obtained) exotic animals and other wildlife products anytime and anywhere (Bell et al., 2004; Marano et al., 2007; Ruysschaert, 2018).

3.2 Overview of pathogens In Table 1 (see appendix) an overview is presented of the diseases connected to IWT based on recent literature. This research shows 126 pathogens, of which 74 or 58.7% are zoonotic.

Most of these emerging diseases are known to be viral (Swift et al., 2007), but the potential of bacterial pathogens must not be underestimated when it comes to spillover caused by bushmeat-related activities (Jones et al., 2008; Kurpiers et al., 2016). Important to highlight is also that the extent of viral and microbial biodiversity is not known yet (Swift et al., 2007), and that potential threads to humans are still to be identified in the future.

Trafficked birds are considered the most important public health concern, since they contribute to 51,6% of zoonotic disease reports in the OIE WAHIS-wild interface (Bell et al., 2004; Can et al., 2018). If only focussing on birds as taxonomic group, low pathogenic was the most reported pathogen (Can et al., 2018). Mammals however, contributed a somewhat same amount (47%) and Pasteurella was here the most reported agent. It should be considered that in some of the studies, e.g. Can et al.

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(2018), the results are based on legal trafficked animals only. The remaining question is whether the diseases reported from legally traded animals give a clear estimate of the disease status of illegally traded animals.

Note that infectious diseases are constantly evolving, and new pathogens can emerge. Information found in the literature may be therefore outdated. Moreover, some of the pathogens are not as well investigated and documented yet compared to others.

3.3 Threats to public health Sixty percent of emerging diseases in humans are zoonotic, of which at least 70% originate from wildlife (Kruse et al., 2004; Karesh et al., 2007; Jones et al., 2008). In this chapter a few examples of zoonotic diseases that find their origin in wildlife will be discussed, with COVID-19 currently emerging. All these examples present pathogens exploiting new host opportunities facilitated by anthropological triggers, which results in the increase of emerging diseases as mentioned earlier.

3.3.1 SARS-related coronaviruses Severe acute respiratory syndrome (SARS) is caused by a divers set of coronaviruses that have an origin in wildlife (Wang et al., 2006). They are known to have caused multiple outbreaks in the twenty- first century: - 2002-2003 SARS-CoV pandemic (Bell et al., 2004). - 2003-2004 SARS-CoV sporadic outbreaks in China (Wang et al., 2006). - 2012-2019 MERS-CoV outbreaks in the Middle East (Zulma et al., 2015). - 2019-… SARS-CoV-2/COVID-19 pandemic (Zhou et al., 2020).

The early cases of SARS in November 2002 occurred in restaurant workers preparing wildlife for human consumption in the Guangdong province in China (Guan et al., 2003; Bell et al., 2004). Over the next months the virus spread to over 30 countries and caused illness in over 7,900 patients (Guan et al., 2003). Because of the suspected relation to bushmeat China reactively banned the consumption of wildlife, but this ban was not permanent (Bell et al., 2004).

In 2003-2004 sporadic outbreaks occurred in the same mentioned region of China, but the causing virus responsible was not identical to the virus isolated in 2002-2003 (Wang et al., 2006). This indicated independent spillover events and predicted future spillover events of SARS-related coronaviruses (SARSr-CoVs) (Wang et al., 2006; Swift et al., 2007). Swift et al. stated in 2007 already that a future pandemic of SARS-rCoV is likely.

In September 2012 another coronavirus emerged; this time with a probable origin in dromedary camels (Zulma et al., 2015). The Middle East Respiratory Virus (MERS-CoV) infection was confirmed in 2494 patients since September 2012 and caused 858 deaths27. Transmission from camels, directly or indirectly via uncondensed camel milk, has been linked to MERS-CoV infection in humans (Zulma et al., 2015).

The most recent outbreak of respiratory coronaviruses is SARS-CoV-2, also called as human coronavirus 19 (hCoV-19), new coronavirus (2019-nCoV) or COVID-1928. This new SARSr-CoV caused an epidemic of acute respiratory distress in humans in the Chinese region Wuhan (Zhou et al., 2020). The virus spread rapidly over the world and since March 2020 the epidemic was declared a pandemic. According to WHO the first confirmed cases in Europe was on February 22 202029, but recent research in Cambridge may suggest otherwise (Mavian et al., 2020).

27 WHO MERS-CoV: https://www.who.int/emergencies/mers-cov/en/; last consultation April 12, 2020. 28 Nature, COVID-19: https://www.nature.com/articles/d41586-020-00154-w; last consultation March 13, 2020. 29 Update of COVID-19 by WHO: https://who.sprinklr.com/; last consultation on April 13, 2020.

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On May 20, which was during the writing-phase of this master dissertation, Belgium counted 55,983 confirmed cases and 9,150 deaths30, showing a significant higher mortality rate than normally observed in Belgium (Fig. 14)31. The latest update of COVID-19 in Belgium can be found in Fig. 1532.

Figure 14 (left) – Mortality in Belgium predicted (grey line and zone) and observed (orange line). From: Epistat Sciensano31. Figure 15 (right) – Current situation in Belgium of COVID-19, last updated on May 20, 2020. It shows the amount hospital beds filled (blue), the number of patients in the intensive care (red), the total amount of deaths (black) and the amount of people that were released from the hospital (green). From: Datawrapper32.

Coronaviridae are enveloped viruses, which contain lipids in their envelop (Nester et al., 2007). This means that they are not very resistant in the outside world. contain 1 molecule of single stranded RNA (Nester et al., 2007). These characteristics are important for the epidemiology of coronaviruses. For example, the fact that it is an RNA virus means that the genome of the virus can mutate quickly (Nester et al., 2017). This is demonstrated in the following graph of GISAID (Fig. 16) for the current epidemic of COVID-19, showing 3123 genomes sampled between December 2019 and April 202033.

Figure 16 – 3123 different genomes of COVID-19 sampled between December 2019 and April 2020, showing the small mutations that occurred in the RNA strain of COVID-19 in these months. The genetic drift is responsible for the ability to eventual infect a person again, even though he/she has been infected before with an earlier variant of this virus. From: GISAID33.

30 Corona virus COVID-19 Global Cases by the CSSE: https://gisanddata.maps.arcgis.com/apps/opsdashboard/index.html#/bda7594740fd40299423467b48e 9ecf6; last consultation May 20, 2020. 31 Epistat Sciensano: mortality in Belgium. https://epistat.wiv-isp.be/momo/; last consultation May 5, 2020. 32 Datawrapper. https://www.datawrapper.de/_/5Aau6/; last consultation May 5, 2020. 33 GISAID: Genomic epidemiology of SARS-CoV-2: https://www.gisaid.org/epiflu-applications/next- hcov-19-app/; last consultation May 5, 2020.

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Genetic variations in critical genes such as the Spike gene contributes to pathogen invasion and adaptation of SARS- corona viruses (Alexander et al., 2018). The Spike gene is translated to the protein responsible for host cell receptor binding (Alexander et al., 2018). The high rate of mutation in critical genes is responsible for the propensity to transmit to other species (Zulma et al., 2015). Other examples within the Coronaviridae are the closely related feline coronavirus-II, canine coronavirus-II and transmissible virus, which are consistent with cross-species transmission (Zulma et al., 2015).

Research revealed that horseshoe bats (Rhinolophus species) are most likely the natural reservoir host of SARS-CoV (Wang et al., 2006). Increased human encroachment in the recent decades have caused bats to become peri-domestic and easily hunted (Kurpiers et al., 2016). The large, sometimes vocal, groups are very susceptible for hunting and popular in the bushmeat trade (Kurpiers et al., 2016). Due to the great genetic diversity of coronaviruses in bats plus the fact that most of them are adapted to one specific species, the native reservoir species of the different SARS-rCoVs is yet not identified (Wang et al., 2006).

Bats are proven to be rich reservoirs for emerging viruses, such as SARS-related coronaviruses (Calisher et al., 2006). Kurpiers et al. (2016) summed up the physiological traits of bats that make them more likely to host and transmit diseases: - Relatively long lifespans, which enables persistent and chronic . - Flight, which allows movement over long distances and generates high temperatures by which viruses may co-evolve. These viruses that can endure febrile temperatures are highly virulent in humans. - High density populations of sympatric species of bats living together, enabling spillover of adapted viruses to other sympatric species. - Regulation of the immune system to host the virus rather than be affected by it.

The role of ‘wet markets’ as amplifying centres becomes clear in the case of coronaviruses. At the wildlife market in Guangzhou in 2002, the horseshoe bats came close to a susceptible amplifier host for SARS-CoV, e.g. the masked palm civet (Parguma larvata) (Kruse et al., 2004; Fèvre et al., 2006; Karesh et al., 2007). A study of Tu et al. (2004) showed a dramatic rise from low or zero prevalence of SARS- CoV in civets at farms to an approximately 80% prevalence in civets tested in markets. The reason why civets are not considered as natural reservoirs is that they develop clinical signs when they are experimentally infected with strains of human SARS-CoV (Wang et al., 2006).

A possible intermediate host of SARS-CoV-2 is also suggested, namely the Malayan pangolin in South China34 (Lam et al., 2020). Pangolins are the most trafficked animals in the world and are sought after for its various body parts (Heinrich et al., 2018). They are often widely present at wildlife markets, such as the one in Wuhan35. The coronavirus that was found to be closely related to COVID-19 – 85.5% to 92.4% genome similarity – could be originated from bats, but a long reservoir state in the pangolins itself could also have been the case (Lam et al., 2020). It requires more research to conclude the role of pangolins in this pandemic, and the true intermediate host remains so far unknown.

Besides the zoonotic aspect, COVID-19 seems to be able to spillback to animals, i.e. felids (domestic and zoo cats36), dogs or ferrets. Shi et al. (2020) found that SARS-CoV-2 can replicate efficiently in ferrets (Mustela putorius furo) and domestic cats (Felis catus), and that the virus is transmittable in cats

34 Nature, Cyranoski, D., 07-02-2020. Did pangolins spread the China corona virus to people? https://www.nature.com/articles/d41586-020-00364-2; last consultation on April 12, 2020. 35 60 Minutes Australia - Journalist goes undercover at "wet markets", where the Coronavirus started, March 8, 2020, on YouTube. https://www.youtube.com/watch?time_continue=6&v=Y7nZ4mw4mXw&feature=emb_logo; last consultation March 23, 2020. 36 OIE WAHIS report of 06/04/20 from the US: one lion and one tiger in a zoo infected with COVID-19. https://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport& reportid=33885; last consultation April 23, 2020.

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via aerosol. In this study both animals developed symptoms after a notable high titre inoculation of the virus (Shi et al., 2020), and therefore it was concluded that the virus may be a health threat to these animals.

The SARSr-CoV outbreaks have an enormous impact on the human population on various aspects. Zoonoses cause illness to a billion people and in a million cases even death, causing a lot of economic damage (Karesh et al., 2012). The outbreak of 2002-2003 in China, for example, costed the economy more than $40 billion (Felbab-Brown, 2017). The World Bank helped in the first half of March 2020 the economy with fourteen billion dollars to protect jobs that were affected by the pandemic of COVID-1937.

Tomas Pueyo states in his article on Medium that, with a pandemic like the current one, collateral damage needs to be taken into account as well38. As the ICU beds are filled with patients suffering from the respiratory distress COVID-19 is causing, those beds are not available to other people that would need intensive care, or the other way around. This means that the normal emergencies can maybe not get the proper care, and this illustrates an additional threat to the public health during a pandemic.

3.3.2 Human Immunodeficiency Virus Another good example of a well-known is the human immunodeficiency virus (HIV) that has his origin in non-human primates (NHPs) that were butchered by bushmeat hunters in Africa in the early 20th century (Kalish, 2005; Karesh et al., 2007). The AIDS pandemic is a reminder of the risk of zoonotic pathogens emerging from wildlife reservoirs to man (Karesh et al., 2012).

Tracing back the HIV viruses has led to the identification of simian immunodeficiency viruses (SIV) as a potential risk to man (Karesh et al., 2012; Kurpiers et al., 2016; Alexander et al., 2018). SIV is closely related to human immunodeficiency viruses (HIV-1 and HIV-2) and both belong to the lentivirus subfamily of (Peeters and Courgnaud, 2002).

This means they convert a single-stranded RNA genome into a double-stranded DNA copy via the enzyme reverse transcriptase (Nester et al., 2007). The viral DNA is then integrated permanently into a chromosome of the host cell (Nester et al., 2007). This way retroviruses are known to have a slow reproduction rate and to cause tumours amongst other pathologies, and in the case of HIV immunodeficiency (Nester et al., 2007).

SIV has been reported in at least 45 African NHPs and is known to have 35 species-specific variants (Peeters and Courgnaud, 2002; Kurpiers et al., 2016). Although SIVs are categorised as immunodeficiency viruses, it does not induce an AIDS-like disease in their natural hosts (Peeters and Courgnaud, 2002). This suggest that these viruses co-evolved with their host. On the other hand, cross- species transmission and co-infection with more than one strain have been frequently documented, sometimes followed by genetic recombination (Peeters and Courgnaud, 2002; Kurpiers et al., 2016). This is an ideal recipe for spillovers to humans (Kurpiers et al., 2016).

The emergence of HIV is the most notable zoonoses that has his origin in wildlife (Kurpiers et al., 2016). It is suggested that the introduction occurred in hunters which had an open wound whilst butchering the NHPs for their meat (Kurpiers et al., 2016). The virus adapted itself to the new human host and diverged from the firstly transmitted virus (Alexander et al., 2018). Of the 35 variants of SIV only a few viruses, from chimpanzees (SIVcpz) and sooty mangabeys (SIVsm), successfully invaded and have persisted in the human host population (Alexander et al., 2018).

37 World Bank, press release March 17, 2020: World Bank Group Increases COVID-19 Response to $14 Billion To Help Sustain Economies, Protect Jobs: https://www.worldbank.org/en/news/press- release/2020/03/17/world-bank-group-increases-covid-19-response-to-14-billion-to-help-sustain- economies-protect-jobs; last consultation March 25, 2020. 38 Tomas Pueyo, Medium, March 19, 2020 https://medium.com/@tomaspueyo/coronavirus-the- hammer-and-the-dance-be9337092b56; last consultation March 23, 2020.

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There is reason to believe that the frequency of SIV exposure and possible infection has increased during the last decade due to the intensifying bushmeat hunting and trade (Kalish et al., 2005). This increase is suspected to be caused by the better access to firearms, increased access to undisturbed NHP habitat from new logging roads, and an increased demand for bushmeat overall (Kalish et al., 2005). These new roads also contribute to the higher probability of emergence (Kalish et al., 2005). Due to the multiple variants and the high prevalence of SIV in the NHP populations, the potential for future and continued spillovers from SIVs is estimated to be high (Kurpiers et al., 2016). However, remarkably, the WHO factsheet of HIV/AIDS is not mentioning anything about the risks of hunting and handling bushmeat39.

3.3.3 Monkeypox During the late spring of 2003 an outbreak of 72 confirmed or suspected human cases with monkeypox occurred in midwestern United States of America (Kruse et al., 2004; Reed et al., 2004). These cases were associated with contact with infected prairie dogs, that were considered pets (Kruse et al., 2004).

The monkey poxvirus is a zoonoses that cause distinct skin lesions (Fig. 17) in humans and typically occurs in Africa (Kruse et al., 2004). Transmission to humans can occur by direct contact with infected animals or their body Figure 17 – Disseminated monkeypox skin lesions in humans, with the morphological fluids (Kruse et al., 2004). differences over time. From: Reed et al., 2004. The outbreak of 2003 is considered a large outbreak compared to outbreaks reported in endemic areas (Reed et al., 2004). In Africa outbreaks are mostly associated with hunting, butchering and eating infected rodents and monkeys (Reed et al., 2004).

Epidemiologic investigation suggested that the prairie dogs had been exposed to imported rodents from Ganda (Kruse et al., 2004; Reed et al., 2004). Via the pet trade the virus was able to spread quickly to captive prairie dogs, and thus to humans, across the USA (Tompkins et al., 2015). Although the most discussed outbreak is the one in 2003, other outbreaks have been documented as well. The first documented case of a human infected with the monkey poxvirus was in 1970 in the Democratic Republic of the Congo, with following infection outbreaks in the surrounding countries (Kurpiers et al., 2016). In the USA, an outbreak occurred in 2007 as well, which epidemiologically was connected to illegally traded rodents, e.g. rope squirrels (Kurpiers et al., 2016).

3.3.4 Zoonotic risks documented in Belgium so far The emergence risk of zoonoses is not limited to developing countries; expanding global trade and travel increase the public health concerns everywhere on Earth (Karesh et al., 2012). Different authors highlighted the illegally imported hawk eagles from Thailand to Belgium that were infected with highly pathogenic avian flu (H5N1), which is, apart from an important zoonosis, also a threat to the domestic and wild birds (Karesh et al., 2005; Fèvre et al., 2006; Pavlin et al., 2009). Chomel et al. (2007) mentions the infection of several custom officers in Antwerp with Chlamydia psittaci after contact with illegally traded birds.

The discussed zoonoses in parts 3.3.1 till 3.3.3 must also be considered as a threat to Belgium specifically. SIVcpz is closely related to HIV-1 and knows 8 different strains (Peeters and Courgnaud, 2002). One of those strains was discovered from a wild-caught animal of Congolese origin, which was intercepted by Belgian customs officers after illegal export from Kinshasa (Peeters and Courgnaud,

39 WHO Factsheet HIV/AIDS: https://www.who.int/news-room/fact-sheets/detail/-aids; last consultation April 13, 2020.

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2002). The researches in the Pano reportage in Oktober 2019 found monkeypox virus in the pieces of bushmeat that was bought in Brussels’ neighbourhood Matonge40.

Apart from the fact that spillover of an infectious disease can occur in Belgium, rapidly spreading diseases such as COVID-19 can enter this country rather easily due to human transport. Also, there was a struggle with taking the necessary measures by the governments in Europe at first, by which the virus had free play at first (Anderson et al., 2020).

3.4 Threats to animal health Most of the literature about IWT contribution to disease spread is focused on the zoonoses and less on the disease that effect the animals of the importing country. However, there are a lot of diseases that form a threat for domestic and native wild animals (Bell et al., 2004). Plus, human activities can be a source of wildlife infection too (Nester et al., 2007; Chomel et al., 2007). An example can be found in an outbreak of Mycobacterium tuberculosis in suricats (Suricata suricatta) and other mongooses (Herpestidae) originating in a human population (Chomel et al., 2007). Transmissions from domestic to wild animals is also possible, being an extra challenge to the survival of endangered species, e.g. canine distemper spreading from domestic dogs to wild canines (Daszak et al., 2000).

3.4.1 Rabies Rabies is the oldest known zoonotic EID and is still an important disease (Kurpiers et al., 2016). The weekly reports of the World Animal Health Information System (WAHIS) of the World Animal Health Organisation (OIE) shows multiple incidents of rabies in the first couple of months of 202041. It is a registered zoonosis in Belgium according to the K.B. of May 22, 2005, and it is an obligation to declare this disease via K.B. of February 3, 2014.

Rabies virus belongs to the Lyssa virus genus, along with Lagos bat virus which is also connected to IWT (Kurpiers et al., 2016). It is transmitted by saliva of a rabid animal into a bite wound or abrasions of the skin, or by inhalation of aerosols containing the virus (Nester et al., 2007). Infected humans have beginning symptoms of fever, head and muscle aches, sore throat, fatigue, and nausea, and will die if not vaccinated in advance (Nester et al., 2007). There are only a few human cases of survival documented (Nester et al., 2007).

This zoonotic virus is widespread in wild animals and is a good example of disease emergence by animal movements (Fèvre et al., 2006; Nester et al., 2007). In bats it can remain latent for a long period in their salivary glands, which makes bats the most important reservoir for spillover to other animals (Nester et al., 2007; Kurpiers et al., 2016). can cause a deadly infection in a variety of wildlife species as secondary or intermediate host, such as NHP species (Kurpiers et al., 2016).

Most human cases may occur from bushmeat-related activities (e.g. bats, NHPs), but are mostly caused by domestic dogs (Kurpiers et al., 2016). In developing countries domestic animals often encounter wildlife and are in danger to be infected with the virus from a wild reservoir (Kurpiers et al., 2016). Dogs excrete the virus for one till three days before showing symptoms and forms thus an unsuspected threat to humans or other animals (Nester et al., 2016).

This can be illustrated by Flores Island in Indonesia, which was free of rabies until 1997 (Fèvre et al., 2006). Three dogs from a rabies endemic area were imported to this island in 1997 (Fèvre et al., 2006). This resulted in 113 human deaths and wiping out of 50% of the dog population in some areas of the island (Fèvre et al., 2006). Translocation of raccoons for hunting purposes in the USA in 1970s also

40 Pano reportage “Aap op het menu”, October 3, 2018: https://www.vrt.be/vrtnu/a-z/pano/2018/pano- s2018a14/; last consultation on March 20, 2020. 41 World Animal Health Organisation (OIE) - World Animal Health Information System: weekly disease information. https://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/WI/index/newlang/en; last consultation on March 8, 2020.

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resulted in a rabies epidemic in the mid-Atlantic states, with thousands of animal cases (Chomel et al., 2007). To control the epidemic, an oral vaccination programmes was launched (Fèvre et al., 2006; Chomel et al., 2007).

Finally, in the late 1970s and early 1980s a rabies epidemic occurred in a kudu (Tragelaphus strepsiceros) population in Namibia (Chomel et al., 2007). After the initial infection by rabid carnivores, the virus spread easily due to the eating preference of the kudu (Chomel et al., 2007). Browsing on thorny trees cause lesions in the oral cavities, which is an entry port for the virus in infected saliva (Chomel et al., 2007).

3.4.2 Bovine tuberculosis Natural and anthropogenic movement of animals influence the epidemiology of another zoonosis caused by Mycobacterium bovis (Kruse et al., 2004). This zoonotic bacterium was supposedly introduced in African wildlife in the colonial area by imported cattle (Kruse et al., 2004). Hereafter the disease became endemic in wildlife and thus an important reservoir for cattle and humans (Kruse et al., 2004; Humblet et al., 2010).

In Ireland and Great Britain bovine tuberculosis is maintained by the reservoir in badgers (Mustelidae), and in New Zealand the wildlife reservoir is known to be in the brushtail possum (Thrichosurus spp.) (Kruse et al., 2004; Fèvre et al., 2006; Chomel et al., 2007). Wild boars and deers can also be infected with M. bovis and consequently recontaminate domestic animals (Kruse et al., 2004; Chomel et al., 2007).

M. bovis is one of the widespread zoonosis that Pavlin et al. (2009) found in their study of imported mammals in the USA during 2000-2005. The reservoir in native wildlife and the wildlife trade can be reasons of why eradication of M. bovis has not been successful so far in some regions (Kruse et al., 2004; Pavlin et al., 2009; Humblet et al., 2010).

3.4.3 Chytridiomycosis Chytridiomycosis is an internationally spread and deadly disease of amphibians that is associated with the international restaurant trade (Bell et al., 2004; Travis et al., 2011). It is caused by fungi of the Batrachochytrium spp.: B. dendrobatidis is causing disease in adult amphibians and B. salamandrivorans in fire salamanders in Belgium, Germany and the Netherlands (Tompkins et al., 2015; Boddy, 2016; Fitzpatrick et al., 2018; Scheele et al., 2019).

The zoospores of B. dendrobatidis penetrate the skin of the amphibians and form sporangia (Boddy, 2016). The colonisation of this chytrid causes epidermal hyperplasia, hyperkeratosis and probably increased skin shedding (Boddy, 2016). The skin is most important for amphibians to maintain their homeostasis, but B. dendrobatidis disrupt the electrolyte transport through the epidermis and therefor causes death (Boddy, 2016).

B. dendrobatidis and rana virus (causing mass mortalities of larval amphibians) are currently on-going emergences that have threaten the amphibians’ survival for the last century (Fèvre et al., 2006; Tompkins et al., 2015). According to some estimations more than one-third of the 6,300 known species of amphibians worldwide are threatened with extinction due to B. Dendrobatidis (Travis et al., 2011; Boddy, 2016).

The farming and transport of living infected amphibians (legal or illegal) are considered as the major pathway of disease spread (Travis et al., 2011). B. salamandrivorans is supposed to be originating from another region of the world and probably been brought into Belgium and the Netherlands via the illegal wildlife trade (Boddy, 2016). It is also suggested that there may be other undiscovered chytrids that can emerge (Boddy, 2016).

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A remarkable connection of the amphibian trade can be made between disease spread and the spread of invasive species, threatening the native biodiversity (Boddy, 2016). If the alien is infected with B. dendrobatidis it can infect the native amphibians in the importing country, logically causing double impact on the biodiversity (Boddy, 2016).

3.4.4 Animal health risks documented in Belgium so far As stated in part 3.3.4, a well-documented example is the highly pathogenic avian influenza brought into Belgium by illegally traded hawk eagles (Karesh et al., 2005; Fèvre et al., 2006; Pavlin et al., 2009). Apart from the public health risk, is H5N1 a great threat for wild and domestic birds in Belgium.

Belgium is officially tuberculosis free since 2003, nevertheless five to ten outbreaks are reported every year (Humblet et al., 2010). Humblet et al. (2010) found no M. bovis circulating in the Belgium wildlife, but this might be caused by a lack of high-resolution data.

Chytridiomycosis is a maintaining threat for amphibians and salamanders in Belgium (Fitzpatrick et al., 2018). Moreover, the TRAFFIC report stated that there were 14,415 live frogs imported in Belgium in the period of 2007-2016 (Musing et al., 2018).

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Discussion This dissertation tries to compile the complex nature of IWT and its consequences. Apart from the rapid decline in biodiversity and the socio-political impact, the risk of emerging disease may be the most important and acknowledged contemporary consequence of IWT. The SARS-CoV-2 (COVID-19) is currently the best example of how IWT has an impact on us all, and not only on the animals and people initially involved.

Recent research showed that Belgium is playing a role in wildlife trafficking, as a significant hub for import, export and transit off wild animals and its derivates (Musing et al., 2016; Chaber et al., 2019). The lack of capacity, financial support and coordinated efforts to tackle wildlife trafficking add to the problem, which was accentuated by the contacted enforcement officers in this study.

For a better understanding of the implementation of CITES-regulation in Belgium, interviews were held with the custom’s Group Anti-Drugs team, who is active at Brussels Airport. Several key problems related to the IWT-control program in Belgium were highlighted by the interviewees and are summarized below: - There is clearly too little capacity to control every luggage item at risk to contain illegally traded animals or derived products. - Luggage in direct transit in Belgium are often not inspected. - Luggage in transit coming from another “low-risk” country (e.g. EU) will not be categorized as “high-risk”, even though it may have originated form a “high-risk” country. - On site collaboration with FASFC inspectors (veterinary officers) is ideal for the veterinary background (e.g. recognizing species or distinct pathogenic lesions) but is rarely the case.

Getting IWT higher on the political agenda in Belgium, is mandatory to respond adequately to above mentioned concerns. The multiple ministries should work together to provide an appropriate budget to fight this illegal activity, not least because it is proven to be a risk for the public and animal health of Belgium. A considerable budget for all CITES enforcement actors will help solving the issues mentioned above, because this would result in a higher level of control. Another related issue is however that sanctions are low and rarely enforced in Belgium (Chaber et al., 2019), making the trade low risk. Therefore, a better enforcement of higher penalties, taking into account the potential risks for public and animal health involved, should be pursued. Consequently, it is clear that the Belgium government should unequivocally engage in a higher listing of IWT on the political agenda.

Multiple researchers debated on possible solutions to combat IWT. Most combine four pillars: policy and legislation, law enforcement, community benefits, and education (Rogan et al., 2016). The first two were covered in the previous paragraphs for Belgium specific. Community benefits are mainly focussed on tourism42 (Rogan et al., 2016). Tourism generates jobs and money to protect the wildlife in biodiverse countries. An important note must be made for the effect COVID-19 lockdown on tourism-funded anti-poaching efforts. No tourism during lockdowns means less money to pay the guards of nature parks43. As a solution, governments may try allocating extra budget to conservation projects, to guarantee Figure 18 – Four pillars of integrated approach solving IWT related problems. From: Rogan et protection of valuable species during the lockdown and to al., 2016. safeguard jobs for the local community.

42 European Commission - Enviroment: The EU Approach to Combat Wildlife Trafficking. Last updated August 7, 2019: https://ec.europa.eu/environment/cites/infographics_en.htm; last consultation on April 17, 2020. 43 Wired. Simon, M., February 2, 2020. The Coronavirus Lockdown Is a Threat for Many Animals, Not a Blessing. https://www.wired.com/story/coronavirus-lockdown-conservation/; last consultation May 14, 2020.

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Nelson Mandela once said: “Education is the most powerful weapon which you can use to change the world”. This brings us to the fourth key focus area. Awareness raising may be the best long-term solution to assist in decreasing IWT. Educational programs on hunting, poaching and consuming wildlife are important in the present and the future. The current pandemic of COVID-19 can be used as an educational example, i.e. the impact the virus has and has had on almost every human being, explaining to the public that diseases like this find their way to humans rather easily by this lucrative trade.

With over 4,900,00 confirmed cases and 323,000 deaths (Fig. 19) COVID-19 is a sad illustration of global disasters that are pending to happen44. Of the 126 pathogens found in recent literature (Tab. 1), over half were zoonotic diseases that are connected to IWT, and this might be an underestimation. A substantial fraction of IWT happens under the radar, allowing no real assessment of the disease risks. It would have been interesting if during the study of Chaber et al. (2019) the confiscated bushmeat was tested on potential pathogens, to know which pathogens came into Belgium via more than 3,600 kilograms of bushmeat every month. Unfortunately, that was not the case, but samples were stored for future analyses (Chaber et al., 2019). It is an important opportunity to collect valuable data.

Figure 19 – Global map of confirmed cases of COVID-19 with legend, last updated on May 20, 2020. From: CSSE44.

All the wildlife-human interactions in the commodity chain of IWT are opportunities for diseases to spill over and may cause the next new pandemic. COVID-19 could be a wake-up call for countries to be more prepared for pandemics – and work preventive – in the future. Nevertheless, so far most countries are merely dealing with the consequences of IWT rather tackle the problem at its origin. Countries should be fighting together to address this complex problem now, rather than dealing with the costly consequences later.

It needs to be more emphasized to governments and the public that IWT is the cause of emerging diseases like COVID-19. Another mentioned consequence of IWT, biodiversity loss, is apparently not urging or relevant enough for world leaders to take more effective action. However, prevention of another pandemic and corresponding lockdowns – with drastic effects on the world economy – may be a stronger motivation, as that is definitely no longer a far-flung event. There is a pleading need for more global supported actions to undermine the criminal organisations involved in IWT. Simply increasing the law enforcement is insufficient to lead to have significant impact. This is because despite there being an

44 Corona virus COVID-19 Global Cases by the CSSE: https://gisanddata.maps.arcgis.com/apps/opsdashboard/index.html#/bda7594740fd40299423467b48e 9ecf6; last consultation May 20, 2020.

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increase in illegal commodity prices, there is no according increase in penalties for those involved in IWT (Hauenstein et al., 2019).

For clarification, a comparison with drug trafficking can be made. Many efforts are being made to keep illegal drugs of the streets. More police efforts to punish users, anyone in possession of drugs and low- end dealers will increase drug prices: it is harder to hide, so more expensive to get (Van Uhm, 2016). Penalties may not increase accordingly, leaving the trade highly lucrative with low risks. Moreover, punishing the dealers at the end of the chain will never be as efficient as arresting the wolves on top of the drug family, so the latter is now the main focus of police efforts against drug trafficking. The same is needed to tackle wildlife trafficking.

A proper risk integrative assessment, resulting in preventive measures, is still lacking, despite of the growing consent of the One-Health theory. The latter theory states that the health of humans, other animals and the environment is all connected, and collaborations between multiple disciplines are needed to improve health overall45. In December 2019, a One World One Health conference was held in Brussels about the bushmeat trade, and reptile and amphibian trade in Belgium46. Smaller groups of multidisciplinary experts established during this conference worked together resulting in policy briefs with usable recommendations. A collaboration of different ministries of the Belgium government will need to put these recommendations into practice.

However, it will not be possible to put a stop to wildlife hunting completely by the four pillars as seen in Fig. 18. There will still be people that depend on bushmeat for their protein source in places where livestock production is not viable (Fa et al., 2009). This is also a reason why a total ban on consuming wildlife is not advisable, despite the health risks. By focussing efforts on reducing the demand and in parallel increasing law enforcement, wildlife hunting may decline to the level of subsistence hunting. It is additionally advisable to educate local people explaining which animals to hunt to cover their own consumption, hereby taking into account the threatened status of species.

Another reason why it may become a challenge to completely eradicate bushmeat hunting, are cultural habits. Perhaps a solution here may be to support local hunters in producing their own livestock. Since extensive livestock husbandry is rarely feasible in tropical forest areas (Fa et al., 2009), there is need to work out alternatives for regular livestock, avoiding the common detrimental effects on wildlife habitats. For example, maybe it is easier to produce poultry in these conditions than keeping ruminants. Poultry has a fast reproduction cycle, i.e. a faster turnover of investment than cows, and can be kept on smaller areas. They are relatively omnivorous, which means their husbandry might be less demanding. There is clearly a need from organisations, being governments and non-governmental organisations (NGOs), to help people to make the change.

At last, I would like to emphasize the shortcomings of this study. A downside of this study was the lacking possibility to sample illegally traded wildlife for detection of possible pathogens. A clearer estimation could have been made to determine the risks in Belgium for public and animal health. Contact with the Belgian Institution of Nature Sciences and the Institute for Tropical Medicine Antwerp, who may have been a help for the latter, was not successfully accomplished. The recent study of Chaber et al. (2019) about bushmeat entering Belgium through Brussels Airport did not conclude an analysis of potential pathogens either. This is consequently considered an important follow-up research opportunity that may help convince the Belgium government to invest in better policies and law enforcement.

Another drawback was that I did not succeed in participating in any initial veterinary check-up once an illegally traded animal entered Belgium. It would have been interesting to do a health check-up of these

45 The One Health Initiative, mission statement: http://onehealthinitiative.com/mission.php; last consultation May 20, 2020. 46 Belgium Biodiversity Platform Conference: Dead or Alive: Towards a sustainable wildlife trade. 3 and 4 December 2019. http://www.biodiversity.be/4854; last consultation May 19, 2020.

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probably stressed out animals, to see first-hand the influence of the harsh transportation methods on the animal, and to make an assessment on his chance of survival.

In conclusion, wildlife trafficking is a complex problem and is not such a far-flung event. It has effects on the biodiversity, human society, public and animal health, and a multi-disciplinary approach is evidently needed to address these threats. Multiple examples show that spillover of pathogens from wild reservoirs can have drastic consequences, COVID-19 being the most recent example. Recent studies also give a few examples of confiscations of illegal wildlife specifically in Belgium, that were contaminated with pathogens that form a threat to both public as animal health. Hopefully, the world will learn from the current pandemic of COVID-19 and will take better measures to stop the illegal wildlife trade.

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References

- Alexander, K.A., Carlson, C.J., Lewis, B.L., Getz, W.M., Marathe, M.V., Eubank, S.G, Sanderson, C.E., Blackburn, J.K., 2018. The Ecology of Pathogen Spillover and Disease Emergence at the Human-Wildlife-Environment Interface. In: Hurst, C.J., The Connections Between Ecology and Infectious Disease, Advances in Environmental Microbiology 5. Springer International Publishing AG, part of Springer Nature 2018, pp. 267-289. - Anderson, R.M., Fraser, C., Ghani, A.C., Donnelly, C.A., Riley, S., Furgeson, N.M., Leung, G.M., Lam, T.H., Hedley, A.J., 2004. Epidemiology, transmission dynamics and control of SARS: the 2002–2003 epidemic. Philosophical Transactions of the Royal Society B, 2004, vol. 359, pp. 1091-1105. - Anderson, R.M., Heesterbeek, H., Klinkenberg, D., Déirdre Hollingsworth, T., 2020. How will country-based mitigation measures influence the course of the COVID-19 epidemic? The Lancet, March 6, 2020, published online: https://doi.org/10.1016/S0140-6736(20)30567-5. - Bayazit, V., 2009. Evaluation on Cortisol and Stress in captive animals. Australian Journal of Basic and Applied Sciences, 2009, vol. 3, no. 2, pp. 1022-1031. - Bell, D., Roberton, S., Hunter, P.R., 2004. Animal origins of SARS coronavirus: possible links with the international trade in small carnivores. Royal Society London, vol. 359, 2004, pp. 1107-1114. - Boddy, L., 2016. Interactions with Humans and Other Animals. In: Watkinson, S.C., Boddy, L., Money, N.P., The Fungi, Third Edn. Elsevier, Academic Press, pp. 293-336. - Braet, L., 2010. De effectiviteit van de internationale en Europese reglementering inzake de illegale handel in bedreigde diersoorten. Masterthesis, Master of Law, Faculty of Law School, University of Ghent, Belgium. - Brashares, J.S., Abrahms, B., Fiorella, K.J., Golden, C.D., Hojnowski, C.E., Marsh, R.A., McCauley, D.J., Nuñes, T.A., Seto, K., Withey, L., 2014. Wildlife decline and social conflict. Science, vol. 345, issue 6195, pp. 376-378. - Cain, D.W., Cidlowski, J.A., 2017. Immune regulation by glucocorticoids. Nature Reviews Immunology, 2017, vol. 17, pp. 233-247. - Calisher, C.H., Childs, J.E., Field, H.E., Holmes, K.V., Schountz, T., 2006. Bats: important reservoirs for emerging viruses. Clinical Microbiolocy Reviews, 2006, vol. 19, no. 3, pp. 531- 545. - Can, Ö.E., D’Cruze, N., Macdonald, D.W., 2018. Dealing in deadly pathogens: Taking stock of the legal trade in live wildlife and potential risks to human health. Global Ecology and Conservation, vol. 17, 2019, e00515. - Chaber, A-L., Gaubert, P., 2019. Report on the illegal importation of meat, including bushmeat, seized at Zaventem airport – 2017/2018. Study accomplished under the authority of the Federal Public Service Health, Food Chain Safety and Environment. - Chen, F., 2015. Poachers and snobs: Demand for rarity and the effects of antipoaching policies. Conservation Letters, 2016, vol. 9, pp. 65-69. - Chomel, B.B., Belotto, A., Meslin, F., 2007. Wildlife, exotic pets, and emerging zoonoses. Emerging Infectious Diseases, vol. 13, no. 1, January 2007, pp 6-11. - CITES Belgium, 2018. Triennial report CITES Belgium 2015-2017. Retrieved at https://cites.org/eng/cms/index.php/component/cp/country/BE/national-reports; last consultation on April 14, 2020. - Daszak, P., Cunningham, A.A., Hyatt, A.D., 2000. Emerging Infectious Diseases of Wildlife – Threats to Biodiversity and Human Health. Science, 2000, vol. 287, no. 5442, pp. 443-449. - Davenport, T.R.B., De Luca, D.W., Jones, T., Mpunga, N.E., Machaga, S.J., Kitegile, A., Phillipps, G.P., 2008. The Critically Endangered kipunji Rungwecebus kipunji of southern Tanzania: first census and conservation status assessment. Oryx, vol. 42, pp. 352-359. - Davenport, T., 2019. Rungwecebus kipunji. The IUCN Red List of Threatened Species 2019: e.T136791A17961368. https://dx.doi.org/10.2305/IUCN.UK.2019- 3.RLTS.T136791A17961368.en. Downloaded on 12 May 2020.

29

- Dewulf, J., 2017. Voorkomen van ziekte. In: Inleiding tot de veterinaire epidemiologie, First Edn. Acco, Leuven, Belgium, pp. 27-50. - Dobson, A.P., 2014. Yellowstone Wolves and the Forces that Structure Natural Systems. PLOS Biology, December 2014, vol. 12, issue 12, e1002025. - Duffy, R., 2016. EU trade policy and the wildlife trade. Report for European Parliament. Belgium. - Duffy, R., St John, F.A.V., Büscher, B., Brockington, D., 2016. Toward a new understanding of the links between poverty and illegal wildlife hunting. Conservation Biology, 2016, vol. 30, no. 1, pp. 14-22. - Fa, J.E., Peres, C.A., 2001. Game vertebrate extraction in African and Neotropical forests: an intercontinental comparison. In: Reynolds, J.D., Mace, G.M., Redford, K.H., Robinson, J.G., Conservation of Exploited Species. Cambridge University Press, Cambridge, UK, pp. 203-241. - Fa, J.E., Juste, J., Burn, R., Broad, G., 2002. Bushmeat consumption and preferences of two ethnic groups in Bioko Island, West Africa. Human Ecology, 2002, vol. 30, pp. 397-416. - Fa, J.E., Currie, D., Meeuwig, J., 2003. Bushmeat and food security in the Congo Basin: linkages between wildlife and people’s future. Environmental Conservation, 2003, vol. 30, pp. 71-78. - Fa, J.E., Ryan, S.L. & Bell, D.J., 2005. Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in Afrotropical forests. Biological Conservation, 2005, vol. 121, pp. 167-176. - Fa, J.E., Brown, D., 2009. Impacts of hunting on mammals in African tropical moist forests: a review and synthesis. Mammal Review, 2009, vol. 39, no. 4, pp. 231-264. - Felbab-Brown, V., 2017. Why the illegal wildlife and drug economies matter. In: The Extinction Market: Wildlife Trafficking and How to Counter It. Oxford University Press, New York, USA, pp. 65-86. - Fell, L.R., Shutt, D.A., 1986. Adrenocortical response of calves to transport stress as measured by salivary cortisol. Journal of Animal Science, 1986, no. 66, pp. 637-641. - Fèvre, E.M., Bronsvoort, B.M. de C., Hamilton, K.A., Cleaveland, S., 2006. Animal movements and the spread of infectious diseases. TRENDS in Microbiology vol. 14, no. 3, March 2006, pp. 125-131. - Feytens, K., 2015. Illegale handel in beschermde dieren- en plantensoorten in België: Een verkennend onderzoek naar aard en aanpak. Masterthesis, Master of Law, Faculty of Law School, Katholieke Universiteit Leuven, Belgium. - Field, H.E., 2009. Bats and Emerging Zoonoses: and SARS. Zoonoses Public Health, 2009, vol. 56, pp. 278-284. - Fitzpatrick, L.D., Pasmans, F., Martel, A., Cunningham, A.A., 2018. Epidemiological tracing of Batrachochytrium salamandrivorans identifies widespread infection and associated mortalities in private amphibian collections. Scientific Reports, 2018, vol. 8, no. 13845, pp. 1-10. - Godoy, S.N., Matushima, E.R., 2010. A survey of diseases in Passeriform birds obtained from illegal wildlife trade in São Paulo City, Brazil. Journal of Avian Medicine and Surgery vol. 24, no. 3, September 2010, pp. 199-209. - Gómez, A., Aguirre, A.A., 2009. Infectious diseases and the illegal wildlife trade. Animal Biodiversity and Emerging Diseases: Annals of the New York Academy of Sciences, no. 1149, 2008, pp. 16-19. - Goyes, D.R., Sollund, R., 2016. Contesting and Contextualising CITES: Wildlife Trafficking in Colombia and Brazil. International Journal for Crime, Justice and Social Democracy, 2016, vol. 5, no. 4, pp. 87-102. - Grimm, T.A., Beer, B.E., Hirsch, V.M., Clouse, K.A., 2003. Simian Immunodeficiency Viruses from multiple lineages infect human macrophages: implications for cross-species transmission. Journal of Acquired Immune Deficiency Syndromes, vol. 32, pp. 362-369. - Harfoot, M., Glaser, S.A.M, Tittensor, D.P., Britten, G.L., McLardy, C., Malsh, K., Burgess, N.D., 2018. Unveiling the patterns and trends in 40 years of global trade in CITES-listed wildlife. Biological Conservation, vol. 223, 2018, pp. 47-57. - Harrison, J.R., Roberts, D.L., Hernandez-Castro, J., 2016. Assessing the extent and nature of wildlife trade on the dark web. Conservation Biology, vol. 30, no. 4, pp. 900-904.

30

- Heiken, K.H., Brush, G.A., Gartland, S., Escallón, C., Moore, I.T., Taylor, E.N., 2016. Effects of long distance translocation on corticosterone and testosterone levels in male rattlesnakes. General and Comparative Endocrinology, vol. 237, 2016, pp. 27-33. - Heinrich, S., Wittmann, T.A., Prowse, T.A.A., Ross, J.V., Delean, S., Stepherd, C.R., Cassey, P., 2016. Where did all the pangolins go? International CITES trade in pangolin species. Global Ecology and Conservation, vol. 8, 2016, pp. 241-253. - Humblet, M-F., Gilbert, M., Govaerts, M., Fauville-Dufaux, M., Walravens, K., Saegerman, C., 2010. New Assessment of Bovine Tuberculosis Risk Factors in Belgium Based on Nationwide Molecular Epidemiology. Journal of Clinical Microbiology, 2010, vol. 48, no. 8, pp. 2802-2808. - Jenkins, P.T., Genovese, K., Ruffler, H., 2007. Broken screens: the regulation of live animal imports in the United States. Report of The Defenders of Wildlife in Washington. - Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L., Daszak, P., 2008. Global trends in emerging infectious diseases. Nature, vol. 451, 2008, pp. 990–993. - Jones, B.A., Grace, D., Kock, R., Alonso, S., Rushton, J., Said, M.Y., McKeever, D., Mutua, F., Young, J., McDermott, J., Pfeiffer, D.U., 2013. Zoonosis emergence linked to agricultural intensification and environmental change. PNAS, May 21, 2013, vol. 110, no. 21, pp. 8399- 8404. - Kalish, M.L., Wolfe, N.D., Ndongmo, C.B., McNicholl, J., Robbins, K.E., Aidoo, M., Fonjungo, P.N., Alemnji, G., Zeh, C., Djoko, C.F., et al., Mpoudi-Ngole, E., Burke, D.S., Folks, T.M., 2005. Central African hunters exposed to Simian Immunodeficiency virus. Emerging Infectious Diseases, vol. 11, no. 12, December 2005, pp. 1928-1930. - Karesh, W.B., Cook, R.A., Bennet, E.L., Newcomb, J., 2005. Wildlife trade and global disease emergence. Emerging Infectious Diseases, vol. 11, no. 7, July 2005, pp. 1000-1002. - Karesh, W.B., Cook, R.A., Gilbert, M., Newcomb, J., 2007. Implications of wildlife trade on the movement of avian influenza and other infectious diseases. Journal of Wildlife Diseases, 2007, vol. 43, no. 3, pp. S55-S59. - Karesh, W.B., Dobson, A., Lloyd-Smith, J.O., Lubroth, J., Dixon, M.A., Bennet, M., Aldrich, S., Harrington, T., Formenty, P., Loh, E.H., Mochalaba, C.C., Thomas, M.J., Heymann, D.L., 2012. Ecology of zoonoses: natural and unnatural histories. Lancet, 2012, vol. 380, pp. 1936- 1945. - Kruse, H., Kirkemo, A., Handeland, K., 2004. Wildlife as Source of Zoonotic Infections. Emerging Infectious Diseases, 2004, vol. 10, no. 12, pp. 2067-2072. - Kurpiers, L.A., Schulte-Herbrüggen, B., Ejotre, I., Reeder, D.M., 2016. Bushmeat and Emerging Infectious Diseases: Lessons from Africa. In: Angelici, F.M., Problematic Wildlife, Springer International Publishing Switzerland, 2016, pp. 507-551 - Lam, T.T., Hon, C., Tang, J.W., 2010. Use of phylogenetics in the molecular epidemiology and evolutionary studies of viral infections. Critical Reviews in Clinical Laboratory Science, 2010, vol. 47, no. 1, pp. 5-49. - Lam, T.T., Shum, M.H., Zhu, H., Tong, Y., Ni, X., Liao, Y., Wei, W., Cheung, W.Y., Li, W., Li, L., Leung, G.M., Holmes, E.C., Hu, Y., Guan, Y., 2020. Identification of 2019-nCoV related coronaviruses in Malayan pangolins in southern China. BioRxiv preprint doi: https://doi.org/10.1101/2020.02.13.945485. - Larkin, M., 2003. Monkeypox spreads as US public-health system plays catch-up. The Lancet Infectious Diseases, pp. 461. - Leakey, R., Lewin, R., 1996. In: The Sixth Extinction: Patterns of Life and the Future of Humankind, First Edn. Bantam Doubleday Dell Publishing Group Inc, New York, USA. - Leroy, E.M., Rouquet, P., Formenty, P., Souquiere, S., Kilbourne, A., Froment, J.M., Bermejo, M., Smit, S., Karesh, W., Swanepoel, R., Zaki, S.R., Rollin, P.E., 2004a. Multiple virus transmission events and rapid decline of central African wildlife. Science, 2004, vol. 303, issue 5656, pp. 387-390. - Leroy, E.M., Telfer, P., Kumulungui, B., Yaba, P., Rouquet, P., Roques, P., Gonzalez, J.P., Ksiazek, T.G., Rollin, P.E., Nerrienet, E., 2004b. A serological survey of Ebola virus infection in central African nonhuman primates. The Journal of Infectious Disease, 2004, vol. 190, issue 11, pp. 1895-1899.

31

- Marano, N., Arguin, P.M., Pappaioanou, M., 2007. Impact of Globalisation and Animal Trade on Infectious Disease Ecology. Emerging Infectious Diseases, December 2007, vol. 13, no. 12, pp. 1807-1809. - Mavian, C., Kosakovsky Pond, S., Marini, S., Rife Magalis, B., Vandamme, A.-M., Dellicour, S., Scarpino, S.V., Houldcroft, C., Villabona-Arenas, J., Paisie, T.K. et al., 2020. Sampling bias and incorrect rooting make phylogenetic network tracing of SARS-COV-2 infections unreliable. PNAS, first published May 7, 2020, doi: https://doi.org/10.1073/pnas.2007295117. - Musing, L., Norwisz, M., Kloda, J., Kecse-Nagy, K., 2018. Wildlife trade in Belgium. Report of TRAFFIC and WWF. - Nester, E.W., Anderson, D.G., Roberts, C.E., Nester, M.T., 2007. Viruses, Prions, and Viroids: Infectious Agents of Animals and Plants. In: Microbiology, a human perspective, Fifth Edn. McGraw-Hill, New York, NY, USA, pp. 337-364. - Okoye, I.C., Ozioko, K.U., Obiezue, N.R., Ikele, B.C, 2015. Intestinal parasitic fauna and zoonotic potentials of commonly consumed wildlife. Helminthologia, 2015, vol. 2, no. 3, pp. 195-204. - Pavlin, B.I., Schloegel, L.M., Daszak, P., 2009. Risk of Importing Zoonotic Diseases through Wildlife Trade, United States. Emerging Infectious Diseases, vol. 15, no. 11, November 2009, pp. 1721-1726. - Peeters, M., Courgnaud, V., 2002. Overview of Primate Lentiviruses and their Evolution in Non-human Primates in Africa. In: Kuiken, C., Foley, B., Freed, E., Hahn, B., Korber, B., Marx, P.A., McCutchan, F.E., Mellors, J.W., Wolinsky, S., HIV sequence compendium. Los Alamos, Theoretical Biology and Biophysics Group, Los Alammos National Laboratory, pp. 2-23. - Reed, K.D., Melski, J.W., Graham, M.B., Regnery, R.L., Sotir, M.J., Wegner, M.V., Kazmierczak, J.J., Stratman, E.J., Fairly, J.A., Swain, G.R, Olson, V.A., Sargent, E.K., Kehl, S.C., Frace, M.A., Kline, R., Foldy, S.L., Davis, J.P., Damon, I.K., 2004. The Detection of Monkeypox in Humans in the Western Hemisphere. The New England Journal of Medicine 350;4, 2004, pp. 342-350. - Ripply, W.J., Beschta, R.L., 2012. Trophic cascades in Yellowstone: The first 15 years after wolf reintroduction. Biological Conservation, 2012, no. 145, pp. 205-213. - Ritchie, B.W., 1995. . In: Avian Viruses: Function and Control. Lake Worth, FL, Wingers Publishing, 1995, pp. 285–312. - Rogan, M., Lindsey, P.A, Mcnutt, J., 2016. Illegal bushmeat hunting in the Okavango Delta, drivers impacts and potential solutions. FAO/Panthera/Botswana Predator Conservation Trust, Harare, pp. 1-62. - Rosen, G.E., Smith, K.F., 2010. Summarizing the Evidence on the International Trade in Illegal Wildlife. EcoHealth 7, pp. 24-32. - Rueda-Cediel, P., Anderson, K.E., Regan, T.J., Regan, H.M., 2018. Effects of uncertainty and variability on population declines and IUCN Red List classifications. Conservation Biology, August 2018, vol. 32, issue 4, pp. 916-925. - Ruysschaert, S., 2018. Background info wildlife trade. Paper for WWF Belgium, Brussels. - Sax, D.F., Brown, J.H., 2000. The paradox of invasion. Global Ecology and Biogeography, 2000, vol. 9, no. 5, pp. 363-371. - Scheele, B.C., Pasmans, F., Skerrat, L.F., Berger, L., Martel, A., Beukema, W., Acevedo, A.A., Burrowes, P.A., Carvalho, T., Catenazzi, A., et al., 2019. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science, 2019, vol. 363, no. 6434, pp. 1459-1463. - Shi, J., Wen, Z., Zhong, G., Yang, H., Wang, C., Liu, R., He, X., Shuai, L., Sun, Z., Zhao, Y. et al., 2020. Susceptibility of ferrets, cats, dogs and different domestic animals to SARS- coronavirus-2. BioRxiv preprint doi: https://doi.org/10.1101/2020.03.30.015347. - Smith, K.M., Zambrana-Torrelio, C., White, A., Asmussen, M., Machalaba, C., Kennedy, S., Lopez, K., Wolf, T.M., Daszak, P., Travis, D.A., Karesh, W.B., 2017. Summarizing US Wildlife Trade with an Eye Toward Assessing the Risk of Infectious Disease Introduction. EcoHealth 14, 2017, pp. 29-39.

32

- Sollund, R., 2016. Wildlife Trafficking in a Globalized World: An Example of Motivations and Modus Operandi from a Norwegian Case Study. In: F. M. Angelici, Problematic Wildlife. Springer International Publishing, Switzerland, pp. 553-570. - Swift, L., Hunter, P.R., Lees, A.C., Bell, D.J., 2007. Wildlife Trade and the Emergence of Infectious Diseases. EcoHealth 4, 2007, pp. 25-30. - Taylor, L.H., Latham, S.M., Woolhouse, M.E., 2001. Risk factors for human disease emergence. Philosophical Transactions of the Royal Society B, 2001, vol. 356, no. 1411, pp. 983-989. - Taylor, G., Scharlemann, J.P.W., Rowcliffe, M., Kümpel, N., Harfoot, M.B.J., Fa, J.E., Melisch, R., Milner-Gulland, E.J., Bhagwat, S., Abernethy, K.A. et al., 2014. Synthesising bushmeat research effort in West and Central Africa: A new regional database. Biological conservation, 2015, vol. 181, pp. 199-205. - Tompkins, D.M., Carver, S., Jones, M.E., Krkošek, M., Skerratt, L.F., 2015. Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology, April 2015, vol. 31, no. 4, pp. 149-159. - Travis, D.A., Watson, R.P., Tauer, A., 2011. The spread of pathogens through trade in wildlife. Scientific and Technical Review of the Office International des Epizooties, 2011, vol. 30, pp. 219-239. - Tu, C., Crameri, G., X. Kong, X., Chen, J., Sun, Y., Yu, M., Xiang, H., Xia, X., Liu, S., Ren, T., Yu, Y., Eaton, B.T., Xuan, X., Wang, L-F, 2004. to SARS coronavirus in civets. Emerging Infectious Diseases, 2004, vol. 10, pp. 2244-2248. - Van Uhm, D.P., 2012. Organised crime in the wildlife trade. Paper for Centre for Information and Research on Organised Crime, Utrecht, The Netherlands. - Van Uhm, D.P., 2016. Enter the Field of Wildlife. In: The Illegal Wildlife Trade, First Edn. Springer International Publishing Switcherland, Willem Pope Institute, Utrecht University, Utrecht, The Netherlands, pp. 75-88. - Vitlec, A., Lord, J.M., Phillips, A.C., 2014. Stress, ageing and their influence on functional, cellular and molecular aspects of the immune system. Age (Dordr), 2014, vol. 36, no. 3, pp. 1169-1185. - Wang, L-F., Shi, Z., Zhang, S., Field, H., Daszak, P., Eaton, B.T., 2006. Review of Bats and SARS. Emerging Infectious Diseases, vol. 12, no. 12, December 2006, pp. 1834-1840. - Warchol, G.L., Zupan, L.L., Clack, W., 2003. Transnational criminality: an analysis of the illegal wildlife market in Southern Africa. International Journal for Crime, Justice and Social Democracy, 2003, vol. 13, pp. 1-26. - Wilson, E.O., 2016. Why extinction is accelerating. In: Half-Earth, First Edn. Liveright Publishing Corporation, New York, USA, pp. 53-63. - Wilson-Wilde, L., 2010. Wildlife crime: a global problem. Forensic Science, Medicine, and Pathology 6, 2010, pp. 221-222. - Wyatt, T., 2013. The Security Implications of the Illegal Wildlife Trade. CRIMSOC: the Journal of Social Criminology, Autumn/Winter 2013, pp. 130-158. - Zhang, L., Hua, N., Sun, S., 2008. Wildlife trade, consumption and conservation awareness in southwest China. Biodiversity Conservation 17, 2008, pp. 1493-1516. - Zhou, P., Yang, X., Hu, B., Zhang, L., Zhang, W., Si, H., Zhu, Y., Li, B., Huang, H., Chen, J. et al., 2020. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature, March 12, 2020, vol. 579, pp. 270-289. - Zimmerman, M.E., 2003. The Black Market for Wildlife: Combating Transnational Organized Crime in the Illegal Wildlife Trade. Vanderbilt J. Transnational Law, vol. 36, pp. 1657–1689. - Zulma, A., Hui, D.S., Perlman, S., 2015. Middle East Respiratory Syndrome. Lancet, vol. 386, no. 9997, pp. 995-1007.

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Appendix Table 1: Overview of pathogens associated with illegal wildlife trade. Zoonotic diseases are marked with an asterisk sign. BM: bushmeat trade CC: climate change, vector range expansion IS: invasive species/introduced species HE: human encroachment or habitat alteration ME: migration or expansion of habitat WAP: wild animal part LAT: live animal trade EID: Emerging Infectious Disease OIE: World Organisation for Animal Health

Geography of Category Pathogen Species affected Movement via Importance References emergence Viral Adenovirus Birds LAT Gómez & Aguirre, 2009 African horse sickness: North of Sahara, Equids, dogs CC, LAT Daszak et al., 2000; Alexander et al., 2018 orbivirus Africa Aleutian mink disease virus Mink IS, LAT Invasive Travis et al., 2011 Aphtae epizooticae Ruminants HE, LAT OIE-listed Travis et al., 2011 Australian bat * Bats, humans HE EID Australia Daszak et al., 2000; Travis et al., 2011 Avian pneumovirus Birds LAT Gómez & Aguirre, 2009 Avian reovirus Birds LAT Gómez & Aguirre, 2009 Bohle iridovirus Anurans, fish LAT Invasive Travis et al., 2011 Canine parvovirus Carnivores HE Invasive Europe, USA Can et al., 2018 Cercopithecine herpesvirus-1 Chomel et al., 2007; Pavlin et al., 2009; Travis et al., Macaques, human RT, HE Serious illness Bali (herpes B)* 2011 Circo viruses Can et al., 2018 Crimean-Congo hemorrhagic Pavlin et al., 2009 fever Duvengahe lyssavirus* Bats, mammals BM, LAT Kurpiers et al., 2016 Gabon 2001- Bell et al., 2004; Leroy et al., 2004ab; Chomel et al., 2002, Sub- Bats, carnivores, EID, high 2007; Karesh et al., 2007; Pavlin et al., 2009; Travis et Ebola virus* BM Saharan Africa, ungulates, primates mortality al., 2011; Karesh et al., 2012; Kurpiers et al., 2016; Indonesia, Alexander et al., 2018 Philippines Elephant endotheliotropic African and Asian Invasive, high LAT Travis et al., 2011 herpesvirus elephant mortality Daszak et al., 2000; Kruse et al., 2004; Pavlin et al., Hantavirus* Rodents, human HE, IS EID USA 2009; Travis et al., 2011; Alexander et al., 2018 Australia 1994, Bats, horse, Daszak et al., 2000; Kruse et al., 2004; Field, 2009; Hendravirus* HE EID Papua New primates Travis et al., 2011; Kurpiers et al., 2016 Guinea

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Geography of Category Pathogen Species affected Movement via Importance References emergence Deer, wild boar, Viral virus* LAT, BM Chomel et al., 2007; Travis et al., 2011 human Bell et al., 2004; Kruse et al., 2004; Kalish et al., 2005; Karesh et al., 2007; Gómez & Aguirre, 2009; Travis et HIV/SIV* Primates BM EID Global al., 2011; Karesh et al., 2012; Kurpiers et al., 2016; Alexander et al., 2018; Can et al., 2018 Travis et al., 2011; Kurpiers et al., 2016 HTLV/STLV-1/3* Primates BM

Kruse et al., 2004; Fèvre et al., 2006; Chomel et al., 2007; Karesh et al., 2007; Gómez & Aguirre, 2009; Influenza A (H5N1/H7N.)* Birds LAT OIE-listed Pavlin et al., 2009; Travis et al., 2011; Tompkins et al., 2015; Alexander et al., 2018; Can et al., 2018; Lee et al, 2019 Junin virus* Rodents HE EID Chomel et al., 2007; Travis et al., 2011 Lagos bat lyssavirus* Bats, mammals LAT EID Travis et al., 2011; Kurpiers et al., 2016 Pavlin et al., 2009; Kurpiers et al., 2016; Alexander et Lassa virus* Rodents, human BM al., 2018 Lymphocytic choriomeningitis Primates, rodents Feed mice High mortality Daszak et al., 2000; Pavlin et al., 2009 virus Machupo virus* Rodents HE EID Travis et al., 2011 Angola 2005, Sub-Saharan EID, high Daszak et al., 2000; Marano et al., 2007; Pavlin et al., * Bats, primates RT, HE Africa, mortality 2009; Travis et al., 2011; Kurpiers et al., 2016 Indonesia, Philippines Daszak et al., 2000; Kruse et al., 2004; Travis et al., Menangle* Pigs, bats, human HE EID Australia 1996 2011 Larkin, 2003; Kruse et al., 2004; Reed et al., 2004; Chomel et al., 2007; Karesh et al., 2007; Marano et al., Monkeys, rodents, Monkeypox* LAT Africa, USA 2007; Pavlin et al., 2009; Travis et al., 2011; Tompkins human et al., 2015; Kurpiers et al., 2016; Alexander et al., 2018; Can et al., 2018 HE (spill over Threat to wild Morbillivirus Carnivores from domestic dogs, ferrets USA, Africa Daszak et al., 2000; Can et al., 2018 dogs) and wolfs Daszak et al., 2000; Gómez & Aguirre, 2009; gewoon Newcastle disease virus* Birds, humans ME, LAT High mortality Canada, USA iets

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Geography of Category Pathogen Species affected Movement via Importance References emergence Daszak et al., 2000; Kruse et al., 2004; Chomel et al., Pigs, dogs, bats, Malaysia 1998, Viral Nipah * HE, ME EID 2007; Jones et al., 2008; Field, 2009; Pavlin et al., 2009; primates Singapore Travis et al., 2011; Kurpiers et al., 2016; Can et al., 2018 Ophidian paramyxovirus Snakes High mortality Daszak et al., 2000 Other pox viruses*, like avian Gómez & Aguirre, 2009; Travis et al., 2011; Can et al., Birds, IS OIE-listed poxvirus 2018 Paramyxovirus 1,2 Birds LAT Invasive Gómez & Aguirre, 2009; Travis et al., 2011 Phocine distemper virus* Harp seals ME, HE Invasive Travis et al., 2011 Pilchard herpes virus American pilchard LAT, WAP Invasive Travis et al., 2011 OIE-listed, Rabbit haemorrhagic disease Worldwide, Rabbits IS invasive, high Daszak et al., 2000; Travis et al., 2011 virus Australia mortality OIE-listed, Rabbit myxomatosis virus Rabbits IS, ME Travis et al., 2011 invasive Daszak et al., 2000; Bell et al., 2004; Kruse et al., 2004; OIE-listed, HE, IS, ME, LAT, Fèvre et al., 2006; Marano et al., 2007; Chomel et al., Rabies* Mammals threat to wild Africa WAP 2007; Gómez & Aguirre, 2009; Pavlin et al., 2009; Travis dogs et al., 2011; Kurpiers et al., 2016 Europe, Daszak et al., 2000; Fèvre et al., 2006; Gómez & Ranavirus Amphibians IS, LAT, WAP Invasive Australia, North Aguirre, 2009; Travis et al., 2011; Tompkins et al., 2015 America Rift Valley fever virus Fèvre et al., 2006; Pavlin et al., 2009 Rinderpest virus Ungulates LAT, HE, ME Invasive Travis et al., 2011 Ruminant gamma herpes viruses (malignant catarrhal Ruminants LAT, HE OIE-listed Travis et al., 2011 fever) Anderson et al., 2004; Kruse et al., 2004; Fèvre et al., Asia 2002-2003, 2006; Wang et al., 2006; Jones et al., 2008; Karesh et Bats, civets, camel, Middle East al., 2007; Field, 2009; Pavlin et al., 2009; Travis et al., SARS-related and MERS felids, pangolin, LAT, BM EID 2012-2019, 2011; Karesh et al., 2012; Kurpiers et al., 2016; Zulma coronavirus* human pandemic 2019- et al., 2015; Alexander et al., 2018; Anderson et al., … 2020; Cowling et al., 2020; Shi et al., 2020; Velavan et al., 2020; Wu et al., 2020; Zhou et al., 2020 Gómez & Aguirre, 2009; Travis et al., 2011; Kurpiers et * Primates LAT, BM al., 2016 Squirrel parapox virus Grey squirrel IS Invasive Travis et al., 2011 Tick-borne encephalitis virus Pavlin et al., 2009

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Geography of Category Pathogen Species affected Movement via Importance References emergence Venezuelan equine Viral Horse CC Pavlin et al., 2009; Alexander et al., 2018 encephalitis virus Substantial Wallal virus Kangaroo spp. Australia Daszak et al., 2000 mortalities USA, Europe, Daszak et al., 2000; Kruse et al., 2004; Travis et al., West-Nile virus* Birds, horse, human ME, HE, LAT EID Africa, Asia, 2011; Tompkins et al., 2015; Can et al., 2018 Australia virus* Primates BE Bell et al., 2004; Pavlin et al., 2009 Bacterial Anaplasma phagocytophilum Deer, rodents Kruse et al., 2004 Kruse et al., 2004; Pavlin et al., 2009; Kurpiers et al., Bacillus anthracis * Mammals BM 2016; Alexander et al., 2018 Rodents, deer, USA, Europe, Daszak et al., 2000; Kruse et al., 2004; Chomel et al., Borrelia burgdorferi HE, LAT, IS EID humans and other Asia 2007; Alexander et al., 2018 Daszak et al., 2000; Kruse et al., 2004; Chomel et al., Brucella spp.* Mammals LAT, HE, WAP Abortion USA 2007; Pavlin et al., 2009; Travis et al., 2011 Belgium, March Chomel et al., 2007; Gómez & Aguirre, 2009; Travis et Chlamydophila psittaci* Birds, human LAT OIE-listed 1994 al., 2011 Clostridium botulinum* Ruminants, human LAT, HE Can et al., 2018 Clostridium perfrigens* Mammals Gómez & Aguirre, 2009 USA, Europe, Daszak et al., 2000; Fèvre et al., 2006; Travis et al., Erhlichia canis* Canids, humans HE EID Africa 2011 Deer, rodents, ticks, USA, Europe, Erhlichia chaffeensis* HE EID Daszak et al., 2000; Kruse et al., 2004 horses Africa USA, Europe, Erhlichia equi* Horses, humans HE EID Daszak et al., 2000 Africa Hares, rabbits, Kruse et al., 2004; Chomel et al., 2007; Pavlin et al., Francisella tularensis* rodents, prairie dog, BM, HE, LAT, IS 2009; Travis et al., 2011 human Daszak et al., 2000; Kruse et al., 2004; Pavlin et al., Leptospira spp.* Rodents, mammals HE, LAT OIE-listed 2009; Kurpiers et al., 2016; Alexander et al., 2018; Can et al., 2018 Listeria monocytogenes* Mammals Can et al., 2018 Mycobacterium avium Wild rabbits, red ME, HE OIE-listed Travis et al., 2011 paratuberculosis deer Kruse et al., 2004; Fèvre et al., 2006; Chomel et al., Mycobacterium bovis* Ungulates, primates HE, IS, LAT OIE-listed 2007; Pavlin et al., 2009; Travis et al., 2011; Alexander et al., 2018

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Geography of Category Pathogen Species affected Movement via Importance References emergence Monkeys, rodents, Bacterial Mycobacterium leprae* HE, LAT Invasive Travis et al., 2011 armadillo Ungulates, Mycobacterium tuberculosis* LAT EID Chomel et al., 2007; Travis et al., 2011 elephants, primates Mycoplasma conjuctivae Alpine chamois IS Invasive Travis et al., 2011 OIE-listed, Daszak et al., 2000; Travis et al., 2011; Tompkins et al., Mycoplasma gallisepticum Birds ME USA invasive 2015 Mass Mycoplasma spp. Tortoises IS USA Daszak et al., 2000 mortalities Pasteurella spp.* Birds LAT Gómez & Aguirre, 2009; Can et al., 2018 Pseudomonas aeruginosa Birds LAT Gómez & Aguirre, 2009 Sub-Saharan Chomel et al., 2007; Jones et al., 2008; Travis et al., Rickettsia africae* Human HE EID Africa, Europe, 2011 North America Daszak et al., 2000; Kruse et al., 2004; Chomel et al., Mammals, reptiles, Mass Norway 1987, Salmonella spp.* LAT 2007; Gómez & Aguirre, 2009; Pavlin et al., 2009; Travis birds mortalities 1999. UK. et al., 2011; Kurpiers et al., 2016; Can et al., 2018 Marine invertebrates, Vibrio cholerae* IS Invasive Travis et al., 2011 oyster-eating fish, humans Rodents, fleas, Panglobal, Daszak et al., 2000; Bell et al., 2004; Pavlin et al., 2009; Yersinia pestis* domestic cats, other HE, IS notably India, Travis et al., 2011; Alexander et al., 2018 mammals USA Hares, rabbits, Yersinia pseudotuberculosis* BM Can et al., 2018 pigs47, humans Invasive, high Fungal Aphanomyces astaci Crayfish IS Europe Daszak et al., 2000; Travis et al., 2011 mortality Aspergillus fumigatus* Birds, human Gómez & Aguirre, 2009 Amphibians, Invasive, mass Daszak et al., 2000; Fèvre et al., 2006; Travis et al., Batrachochytrium spp. IS, RT Panglobal salamanders mortalities 2011; Tompkins et al., 2015 Parasitic Ancylostoma spp.* Humans BM Panglobal Okoye et al., 2015 Ascardia galli* Birds BM Okoye et al., 2015

47 Medscape: Pseudotuberculosis (Yersinia pseudotuberculosis Infection). Author Haburchak, D.R., Updated October 11, 2017. https://emedicine.medscape.com/article/226871-overview#a1; last consultation March 18, 2020.

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Geography of Category Pathogen Species affected Movement via Importance References emergence Parasitic Ascaris lumbricoides* Humans BM Panglobal Okoye et al., 2015 Balantidium coli* Primates BM Kurpiers et al., 2016 Birds, reptiles, Capillaria bursata* BM Okoye et al., 2015 humans Cediopsylla simplex Carnivores Gómez & Aguirre, 2009 Cattle, rodents, Cryptosporidium parvum* HE, LAT Europe, USA Daszak et al., 2000; Alexander et al., 2018 other mammals Dicrocoelium hospes* Humans BM Okoye et al., 2015 Kruse et al., 2004; Fèvre et al., 2006; Gómez & Aguirre, Echinococcus multilocularis* Carnivores BM, IS OIE listed 2009; Pavlin et al., 2009 Eimeria tenella* Birds BM Okoye et al., 2015 Entamoeba histolytica* Mammals BM Okoye et al., 2015; Kurpiers et al., 2016 Enterobius vermicularis* Humans BM Okoye et al., 2015 North American Fascioloides magna IS Invasive Travis et al., 2011 wapiti Giardia intestinalis* Birds, mammals BM Gómez & Aguirre, 2009; Kurpiers et al., 2016 Globocephalus diducta* Humans BM Okoye et al., 2015 Haemoproteus spp. Birds Gómez & Aguirre, 2009 Heligmosomoides polygyrus* Rodents BM Okoye et al., 2015 Hymenolepis nana* Humans BM Okoye et al., 2015 Isospora spp. Carnivores Gómez & Aguirre, 2009 Leishmania spp. Wild canids HE, LAT OIE-listed Brazil Fèvre et al., 2006; Travis et al., 2011 Leucocytozoon spp. Birds Gómez & Aguirre, 2009 Metastrongylus elongatus* Humans BM Okoye et al., 2015 Moniliformis moniliformis* Humans BM Okoye et al., 2015 Europe, USA, Myxobolus cerebralis Salmonid fish IS High mortality Daszak et al., 2000 Africa Canids, ruminants, Neospora caninum* ME, HE Invasive Travis et al., 2011 felines Oesophagostomum Humans BM Okoye et al., 2015 columbianum Opisthorchis spp.* Fish, humans BM Gómez & Aguirre, 2009 Otodectes cynotis Carnivores LAT, HE Gómez & Aguirre, 2009 Plasmodium spp.* Birds, human IS High mortality Daszak et al., 2000; Travis et al., 2011; Can et al., 2018 Pseudamphistomum truncatum Fish, canids, felines IS Invasive Fèvre et al., 2006; Travis et al., 2011 Pulex simulans Carnivores HE, LAT Gómez & Aguirre, 2009

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Geography of Category Pathogen Species affected Movement via Importance References emergence Carnivores, other Parasitic Sarcocystis spp. BM, LAT Gómez & Aguirre, 2009 mammals Australia, UK, Sarcoptes scabiei* Mammals HE, LAT EID Can et al., 2018 Sweden Steinhausis spp. Partula snails IS, LAT Invasive Daszak et al., 2000; Travis et al., 2011 Mammals, birds, Strongyloides spp.* BM Kurpiers et al., 2016 reptiles Taenia saginata Humans BM Okoye et al., 2015 Marine mammals, rodents, felids, BM, LAT, HE, EID, high Daszak et al., 2000; Chomel et al., 2007; Travis et al., Toxoplasma gondii* ruminants, lemurs, ME mortality 2011; Can et al., 2018 marsupials, primates Trichinella native* Bears BM OIE-listed Chomel et al., 2007; Travis et al., 2011 Trichomonas spp. Birds, reptiles Gómez & Aguirre, 2009; Can et al., 2018 Trichostrongylus retortaeformis Humans BM Okoye et al., 2015 Trichuris trichiura Reptiles, mammals BM Okoye et al., 2015 Trypanosoma brucei Vertebrates LAT, ME Uganda Alexander et al., 2018 rhodesiense* Panglobal, except Varroa jacobsoni Honey bee IS OIE-listed Daszak et al., 2000; Travis et al., 2011 Australasia and Central Africa Ungulates, felids, Prions BSE e.g.* BM High mortality Kurpiers et al., 2016 primates

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