Regulatory approaches governing wildlife trade.

Regulatory approaches governing wildlife trade aim to strike a balance between supporting legitimate and sustainable trade for conservation purposes while preventing illegal trafficking and protecting threatened species. These approaches can differ between countries, but there are some common elements and international agreements that influence wildlife trade regulations, in particular the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). CITES is an international treaty that came into effect in 1975 and is one of the most crucial regulatory frameworks for wildlife trade. Its goal is to ensure that international trade in wild animal and plant species does not threaten their survival. However, individual countries enact their own wildlife laws and regulations to govern domestic trade and protect their native species. These laws may specify which species are protected, which are allowed for trade, and the permits or licenses required for legal trade.

Establishing the legality of wildlife trade can be difficult, however. For Toland et al. [41], the distinction between legal and illegal trade between countries can be problematic, as trade considered legal or illegal in one country may be the opposite from the viewpoint of another country’s legislation. Romero-Vidal et al. [42] found that the legal export of parrots may be maintained while the domestic capture of parrots as companion pets is prohibited among neotropical countries (approx. 46 countries in Central and South America, including Mexico); or parrots as crop pests may be legally hunted while keeping parrots as pets is prohibited. In some cases, issues are also in evidence domestically: wildlife trade regulations in China were found not to function as expected given outdated protected species lists, insufficient cross-sector collaboration, and weak restrictions and law enforcement for the farming and trading of species [43].

China’s 2020 decision to ban the trade and consumption of terrestrial wild animals [19] also features inconsistencies between China’s Protected Species List and the extinction risks set by CITES and the International Union for Conservation of Nature (IUCN) [44], demonstrating the gap between the scientific justifiability of the ban on conservation grounds [45]. This ban excluded species with zoonotic spillover potential such as bats, which raises concerns as bats are the suspected reservoir of SARS-CoV-2 and the natural reservoir for a range of coronaviruses [44], and highlights the need for research addressing the nexus between bushmeat, wet markets and disease within a One Health (OH) framework [46].

Wildlife trade also underlies traditional medicine and exotic pets. The United Nations Environment Program (UNEP) and International Livestock Research Institute (ILRI) cite global trade in traditional medicine and exotic pets as one of the reasons for the expanding human-animal-environment interface within which zoonotic spillover is facilitated [20]. Toland et al. and Neuwirth et al. [41, 47] argue that the regulation of traditional medicines and exotic pets is plagued by problems of fragmentation and a lack of oversight.

Neuwirth and Svetlicini [47] highlight the patchwork nature of international law (eg, conflicts of laws) and compare this to the subdivision and specialization of international legal regimes. Viens et al. [48] similarly find a lack of consensus and devolution of the definition, categorization, and governance of animals within international law to different individual governance systems, leading to a fragmented approach to the regulation of human-animal interactions related to zoonoses.

One of the biggest challenges for governing wildlife trade is the fragmentation of authority and ambiguity of regulation. For Huang et al. [44], China’s 2020 Wildlife Protection Law provides ambiguous legal provisions where restricted wildlife may still be used commercially for fur, traditional medicine, and captive breeding. Similarly, Chen et al. [49] find that a lack of specificity in defining what is exempt from China’s ban on trade in ivory may enable the legal importation and trade in ivory despite such items being illegal. D’Cruze and Macdonald (2015) call for extending the ban on the Asian big cat trade to include commercial trade in captive bred individuals given the increase in illegal poaching of clouded leopard parts for traditional medicine [50]. To address the fragmentation and lack of oversight in the global trade of amphibians as pets, Borzee et al. [26] recommend regulating the movement of such amphibian species that can spread pathogens through the global pet trade to prevent zoonotic spillover.

Regulatory approaches governing human consumption of wildlife through bushmeat trade.

The regulation of domestic bushmeat hunting, farming, selling, trading, purchasing, and use varies in legislative environment and legal requirements according to each country. Despite the existence of legislation to prohibit the importation of bushmeat across countries, regulatory efforts are hindered by gaps in enforcement and a lack of consensus on terminology.

Chaber et al. [51] notes that animal health legislation and wildlife trade legislation exists in the European Union that prohibits the import of bushmeat from third-party countries into the EU where such bushmeat belongs to CITES annex-listed species. However, the authors note that there is no general established practice in the EU for seizing illegal bushmeat, making the enforcement of these regulations through investigation of alleged offenses and securing evidence for prosecution difficult.

Svensson et al. [52] found that there is some level of protection for galago primates, a species that is consumed as bushmeat, in the respective national legislations of countries in the galago range as per the countries’ CITES obligations. However, authors found that galago trade regulations vary in protection due terminology issues resulting in significant differences in meaning, outdated and/or incorrect taxonomy within respective legislation, and due to the reliance on subsidiary regulations that have not been implemented and/or administrative agencies that were not yet formed [52].

In Colombia, Van Vliet et al. [53] found that commercial bushmeat hunting continues despite the de facto inability to obtain commercial permits for bushmeat hunting because of conflicting legal authorities, a lack of technical capacity, and a lack of guidance. Autonomous Regional Corporations are unable to exercise their legal authority to refuse the issuing of commercial hunting licenses in their jurisdiction because the national Ministry of Environment has not published a list of species permitted to be harvested within a given global harvesting quota, of which the Ministry of Environment is entitled to set by national Decrees. The national Ministry of Environment and the Autonomous Regional Corporations have also not developed the formal criteria and methodologies to monitor hunted species and to estimate the available stocks that are required to issue hunting licenses. Furthermore, sanitary regulations for the handling of bushmeat and its processing are yet to be defined by the Ministry of Health and Social Protection, such that bushmeat cannot be legally commercialized for human consumption [53].

In the city of Sekondi-Takoradi, Ghana, bushmeat trade was found to be largely unregulated by state or local institutions, with no evidence of any individual actors or actor groups exerting control over the bushmeat market [54]. Absent actors with regulatory functions include the local police which issue licenses for shotgun use, the wildlife department which issues licenses for bushmeat hunting, district assemblies which issue licenses for bushmeat trade, third-party actors such as hunter unions, guilds, or associations that would provide some level of regulation, representation, and arbitration [54].

In Southern Africa, various transfrontier conservation area structures exist to promote cooperation amongst multiple countries in the management of contested shared natural resources, including wild animals, migratory species, and pastures for livestock rearing [55].

The existence of such transfrontier conservation area structures demonstrates functional collaboration among stakeholders [55], however transfrontier conservation areas in sub-Saharan Africa may increase the risk for incursion of Trichinella spp. into the human food chain by increasing the association of wildlife with domestic animals in rural areas at the edge of protected areas, and therefore the risk of Trichinella spp. infection in humans [56].

Regulatory approaches governing use of wildlife for traditional medicine trade.

The following section relies on the single study found on regulatory approaches governing use of wildlife for traditional medicine trade. Table 1 below summarizes information describing the international legal regimes regulating traditional medicine.

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Table 1. The international legal regimes that regulate traditional medicine.

https://doi.org/10.1371/journal.pone.0312012.t001

Regulatory approaches governing use of wildlife for traditional medicine trade aim to address the potential impacts on wildlife conservation and animal welfare while respecting cultural practices and traditional knowledge. The trade of animal parts and derivatives for use in traditional medicine has been a significant concern due to its contribution to illegal wildlife trafficking and threats to endangered species.

Traditional medicine is increasingly dominated by western governance arrangements that regulate relations between health, trade, and intellectual property rights, and, as such, is subject to similar degrees of harmonization and fragmentation [47]. CITES also plays a crucial role in regulating the international trade of animals and plants used in traditional medicine. The treaty categorizes species into different classes (Appendices I to III), with varying levels of protection, and stipulates that permits are required for the international trade of species listed under Appendix I and II, ensuring that trade is legal and sustainable. In addition, some countries maintain positive lists that identify which animal parts and products can be legally used in traditional medicine. These lists often exclude endangered species and only include species that are abundant and can be sustainably sourced.

Traditional medicine has been described by Neuwirth and Svetlicini [47] as regulated within a public health environment where the dominant Western pharmaceutical model of health care increasingly includes the practice of traditional medicine, now categorized as “medicinal products”. The authors pose that the globalized nature of the market for medicinal products and other health-related goods converge as two distinct models of health care (i.e. a Western pharmaceutical model of health care and traditional medicine). Finally, the authors do not link traditional medicine or traditional medicines containing or being derived from animals or animal parts with zoonotic spillover, zoonotic infection transmission.

Regulatory approaches governing exotic pet trade.

Legislation concerning both the trade and possession of exotic pets in the European Union, the United States, and Canada is analyzed by Toland et al. [41] who highlight the fragmentation and lack of oversight by a single authority. Authors linked trade in exotic pets and their ownership with zoonotic infection transmission, but not zoonotic spillover (see panel for definition), where they define zoonotic infection transmission as the incidence or end result of human infection with animal-based diseases (e.g. salmonellosis) [41].

The CITES is also the primary instrument regulating the international trade in exotic pets [41] included in their list. The Convention identifies wildlife species that may be legally traded, in what quantities, and under which conditions (idem), whereas the Bern Convention on the Conservation of European Wildlife and Natural Habitats and the Bonn Convention on the Conservation of Migratory Species of Wild Animals strengthens the legally binding nature of provisions within CITES for states that are a party to both conventions.

At the national level, legislation regulates trade in exotic pets through implementation of the above conventions and, where applicable, further limits the human-exotic pet interface from hunting to possession or ownership [41]. Such additions to international standards are permitted so long as the national standards are more stringent and scientifically justifiable [45].

Although national-level regulations are therefore compatible with the minimum required by international regulations, Toland et al. [41] argue that a lack of harmonization exists regarding which species’ trade is expressly prohibited, resulting in a legal gap where some species’ trade are targeted systematically, and prohibited only nationally and not internationally by CITES. This can be observed in the case of continued international trade in the Australian shingleback lizard [57] despite strict regulation of the species’ trade domestically in Australia, and no international recognition of this domestic protection.

There is also a lack of inter-state harmonization for regulations regarding the trade in exotic vertebrate pets between the domestic and national levels. Pratt et al. [58] found that state-level governments in the United States have implemented regulations that permit trade in exotic vertebrate pets that are banned from international/national import into the United States due to public health and conservation concerns. Once exotic vertebrate pets have been imported into the United States, inconsistent domestic regulations facilitate the movement of exotic vertebrate pets that pose substantial invasion and disease risks (ibid). Pratt et al. [58] also found that definitions and classifications for regulating different vertebrate taxa varied greatly across state-level governments in the United States, and the terms ‘pet’ and ‘companion animal’ were poorly defined and inconsistent across states, further facilitating the continued possession of exotic pets in states where these animals are banned.

In the case of the poaching and international trade in parrots, differences in the timing of national implementation of international wildlife legislation (i.e. CITES) varied between countries in Central America, the Caribbean, and South America, allowing protected parrot specie trade, keeping as pets, and poaching, presumably until countries ratify and implement the Convention [42].

Beyond the potential incompatibility between national and international regulations, challenges in the regulation of the exotic pet trade are similar to those identified above for wildlife and traditional medicine trade, in particular the fragmented nature of the regulatory landscape.

Institutional mandates: Wildlife species survival, animal health and movement.

CITES regulates international wildlife trade to support wildlife species’ survival. CITES categorizes wildlife species into three appendices depending on the risk that international trade would have on the species’ survival. Based on these appendices, the tradable quantities (i.e. quotas) of wildlife species and their products are determined. Each of these CITES appendices has associated permits and other requirements which must be met for international trade to be legal and non-detrimental to the species’ survival [60]. The appendices, their descriptions, and relevant importation requirements can be found in Table 3. CITES also conducts a significant trade review, which reviews Appendix II (listed species traded in significant quantities), and provides recommendations for the species listed in Appendix I [60]. In keeping with the SPS agreement, states are obligated to base their relevant national measures on the standards developed by CITES.

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Table 3. CITES appendices [45].

https://doi.org/10.1371/journal.pone.0312012.t003

By defining enforcement as the ability to ensure compliance, Cooper and Rosser [45] determined CITES’ enforcement ability as successful due to trade sanctions that moved parties towards compliance in writing. A caveat is that compliance requirements are low, and many parties only meet CITES’ basic requirements. In the case of seahorses, for example, Foster and Vincent [61] found that the CITES’ significant trade reviews lack specificity and metrics for tracking compliance with Review recommendations, and are based on the precedents set by other species.

Developing guidance that ensures consistency in the implementation of CITES provisions as well as expanding legal definitions and approaches would address such compliance issues [26, 62–64]. Foster and Vincent [61] recommend 1) the focus of the CITES Review be shifted from outputs to outcomes and impacts; 2) match CITES Review recommendations to the needs and capacities of the Parties; 3) give experts a formalized role in the CITES Review process; and 4) create funding mechanisms for the Review process, the integration of experts in the Review process, and for assisting Parties in addressing the recommendations from the Review. However, Thiermann [65] argues that global commitment and political will are needed to address compliance issues rather than additional science-based international standards or improved dispute resolution mechanisms.

The WTO recognizes WOAH (formerly OIE) as the reference organization for zoonoses and terrestrial and aquatic animal health in international trade [45]. The WOAH sets animal and aquatic animal health international trade standards for wildlife products to ensure animal health and welfare. While WOAH is explicitly concerned with zoonoses, the focus is more on controlling re-emerging events and surveillance rather than preventing the spillover of new or emerging zoonotic pathogens from being transmitted [65]. The various WOAH documents, their descriptions and relevance can be found in Table 4. In keeping with the SPS agreement, states are obligated to base their relevant national measures on the standards developed by WOAH.

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Table 4. WOAH regulations, standards, and evaluation for international wildlife trade [45, 66].

https://doi.org/10.1371/journal.pone.0312012.t004

Finally, IUCN (formerly World Conservation Union) regulates the international wildlife trade through the provision of guidelines and best practices related to the movement and welfare of animals [45]. However, the IUCN’s guidelines are non-legally binding, and thus, the implementation of and compliance with such standards are less likely than with instruments that provide economic or reputational repercussions for non-compliance. Cooper and Rosser [45] list the following documents as the relevant guidelines and best practices of the IUCN:

1. IUCN Guidelines for the Prevention of Biodiversity loss caused by Alien Invasive Species
2. IUCN/Species Survival Commission Guidelines for Re-Introductions and Other Conservation Translocations
3. IUCN Guidelines for the Placement of Confiscated Animals Closely Related to CITES Resolution Conf. 10.7: Disposal of Confiscated Live Specimens of Species
4. IUCN Policy Statement on State gift of animals
5. IUCN Position Statement on Translocations of Living Organisms: Introductions, Re-Introductions, and Re-Stocking
6. IUCN Policy Statement on Captive Breeding

Institutional mandate: Limit harmful introduction of invasive alien species.

While plant pathogens have been widely overlooked in discussions about global disease spread, Kim et al. highlight instances of illness in humans caused by various bacterial phytopathogens, and the potential for opportunistic pathogens to develop infection strategies of spillover across kingdoms, challenging the notion that plant pathogens are not causative agents of disease in humans and animals [67]. This led Kim et al. to consider the trade in plants and to include the IPPC in their analysis.

The IPPC regulates the international wildlife trade by developing standards to prevent the introduction, spread, and establishment of plants that could become invasive [68]. Such standards may be found in the International Standards for Phytosanitary Measures, which also include glossaries and risk analysis guidance [68]. While the Convention is only legally binding for those states who choose to be a party to the Convention, WTO parties must base their national measures on the standards developed within the Convention as per the WTO SPS Agreement [45]. The IPPC is recognized by the WTO as the reference organization for phytosanitary standard-setting related to trade [68].

With regard to the prevention of zoonotic spillover to infection transmission between humans, Zhang et al. and Chinchio et al. [69, 70] highlight potential for zoonoses from introduced alien species. In order to effectively prevent invasion risks and indirectly prevent zoonotic spillover, Reino et al. argue that global bans are needed as opposed to current regional bans such as those in the European Union [71]. Towards limiting the harmful introduction of invasive alien species, the IPPC cooperates with the CBD. The CBD encourages state parties to regulate the international movement of genetic material to both limit invasive alien species (IAS) and to protect biodiversity, thereby affecting the regulation of the international wildlife trade [45]. While legally binding, the Convention has taken a ‘soft’ approach toward implementation, developing instruments that are not backed by legal obligations to implement [72]. Both the IPPC and the CBD do not directly address the prevention of zoonotic disease, although their respective mandates are part of the trade standards, regulations and incentives that govern the international wildlife trade.

Indirect prevention of zoonotic spillover; prevention of infection transmission between humans (WOAH, FAO, WHO).

The United Nations Food and Agriculture Organization (FAO), WHO and WOAH engage directly in the prevention of zoonotic infection transmission through tools aimed at surveillance, prevention and containment. The Global Early Warning System for Animal Disease is a surveillance system that tracks animal diseases and zoonoses as a joint WOAH/FAO/WHO initiative [73]. Through the International Health Regulations (IHR), the WHO provides a legally binding instrument for state parties to notify, assess, and contain public health emergencies of international concern (PHEIC) [64]. While the IHR do not expressly mention zoonotic disease, the scope of what constitutes a PHEIC is broad so as to cover any incident involving the international spread of diseases requiring a coordinated international response, including zoonotic spillover and resulting infections [64].

Regulation of the movement (trade) of wildlife (CITES, CBD).

Institutions may prevent zoonotic infection transmission through their role in regulating the international movement of flora and fauna. CITES regulates the international wildlife trade through its three appendices (see Table 2) that separate wildlife species according to requirements for import, export, and re-export to address species survival in international trade [62]. Although CITES has no mandate over zoonoses, by regulating the trade and movement of wildlife, it influences factors that may lead to zoonotic spillover, such as animal welfare and biological diversity [34]. The CBD regulates the international movement of genetic material to protect the biological diversity of countries through the similarly named Convention [45]. In parallel, the IPPC controls and prevents the international spread of pests (invasive alien species) and plant diseases [68].

Harmonization of state practice with international standards, policy and practice (WOAH, CITES, WTO, WHO, IUCN, IPCC).

Institutions prevent zoonotic infection transmission through their role in setting international standards, which guides legislation and practice of state parties and non-governmental organizations. WOAH sets international trade standards (trade quotas) through the Terrestrial Animal Health Code and the Aquatic Animal Health Code [45]. Similarly, CITES provides legally-binding requirements for the international trade of wildlife within the CITES appendices, as mentioned earlier. State parties are legally obligated to consult and base their practices and legislation on the respective WOAH and CITES guidelines, depending on the commodity traded and the animal disease(s) of concern [45]. IUCN provides guidelines on aspects related to the movement and welfare of wildlife within international wildlife trade [45]; these guidelines are however non-legally binding and non-enforceable.

In March 2024, CITES and WOAH signed a Memorandum of Understanding [74], catalyzing their collaboration to reduce the risk of zoonotic disease emergence associated with international wildlife trade through a joint programme of work focused on training, capacity-building, networking, coordination and communication. Key areas of mutual interest include the safe, traceable, and legal international trade in wild species of animals, identification of zoonotic disease risks associated with CITES listed species and activities, and facilitation of secure transport for biological samples from wild animals. In May 2024, WOAH published voluntary guidelines for addressing zoonotic spillover risk in wildlife trade spanning the sub-national, national, regional, and international scales [30]; wildlife, domesticated animals, and humans spanning the entire supply chain in a wildlife trade system including wild animal markets, wildlife markets, wet markets; and uses including bushmeat, exotic pets, and traditional medicine. A framework is provided for authorities with a mandate related to animal health and welfare, public health, or wildlife management and trade to assess risk and identify risk-management strategies for wildlife trade guided by a precautionary approach.

The IPPC sets standards related to the environment and biodiversity to help state parties harmonize their management of invasive alien species related to plants [68]. In this way, the role of the IPPC transitions from the standard setting role of institutions such as the WOAH and the CITES Secretariat to the harmonizing and coordinating roles of the WTO and the Codex Alimentarius Commission.

The WTO enforces the harmonization of national measures with international animal health laws and trade rules by providing dispute settlement for trade disputes between state parties [45]. The Codex Alimentarius Commission promotes the coordination of the food standards undertaken by international governmental and non-governmental organizations [68]. The WHO’s IHR may be viewed as international standards regarding disease surveillance, notification and control that direct state action given their legally binding nature [64].

Information sharing and disease control capacity building (WOAH, CITES).

Institutions prevent zoonotic spillover and infection transmission among humans through their role in facilitating capacity building for states, especially concerning disease prevention surveillance and control efforts. WOAH facilitates capacity building for states, especially in mainstreaming veterinary services and veterinary public health as a key part of the national and international response to the international wildlife trade and animal disease prevention and control, as well as information sharing amongst state parties regarding expertise and best practices [73]. Similarly, WOAH certifies the competence and credibility of national veterinary services through the Tool for Evaluation of Performance of Veterinary Services (WOAH-PVS Tool) and facilitates capacity building in national veterinary services to promote trust amongst international trading partners and ensure the international wildlife trade fosters public and animal health [73]. TRAFFIC, the Wildlife Trade Monitoring Network, acts as a source and facilitator of research and data regarding the trade status of, and threats to CITES species; reports on prosecutions for illegal trade; and CITES enforcement activities globally [45].