Major drivers of human–animal contact allowing pathogen exchange include animal domestication for companionship and food production, anthropocentric alteration of the environment and the global movement of animals and goods. Approximately one-quarter of human deaths are caused by infectious disease and nearly 60% of infectious diseases are considered zoonotic (pathogens transmissible between animals and humans); most of these (>70%) are caused by pathogens of wildlife origin (Taylor et al. 2001; Jones et al. 2008; Drexler 2010). Whereas historically disease spillover events were likely to remain local, even undetected due to natural, cultural and geographic barriers, modern transportation allows emerging diseases to spread along various globally connected networks in a matter of days. In the past decade alone, we have witnessed several novel disease threats to global health, food security and economic stability as a result of one of these networks—the trade of live wild animals and/or their products (Karesh et al. 2007, 2012).
Anthropogenic movement and manipulation of domestic and wild animals, including globalized trade, were proposed as “the” biggest potential trigger drivers for disease emergence and spread since the advent of agriculture [WHO, Food and Agriculture Organization (FAO) and World Organisation for Animal Health (OIE) joint report 2004]. Lack of wildlife trade surveillance and proper systematic management of the data available represents a major gap to understand and determine high-risk pathways of potentially adverse organisms’ introduction. In order to properly assess this threat to the USA, we must (1) better understand the scope of the trade in terms of species, volume, condition and origin; (2) determine high-risk pathways of introduction for further assessment; and (3) understand the regulatory framework that exists to manage these threats.
The goal of this study is to characterize the wildlife trade entering the USA as a baseline for understanding the magnitude of the potential threat these activities may pose to the environment, animals and humans. Although reports exist in the literature, to our knowledge this is the broadest summary (in terms of time scale and detail) aimed at supporting risk assessments surrounding US wildlife trade importation.
The Global Wildlife Trade
Wildlife trade is one of the largest and most complex commerce exchanges in the world. The legal global trade in wildlife and wildlife products involves the movement of billions of plants and animals comprising an economic value estimated at US $300 billion per annum (Ahlenius 2008; WWF/Dalberg 2012). The illegal aspect of wildlife trade is estimated to be a $5–20 billion-dollar industry, comparable to the international trade of narcotics and weapons (Wyler and Sheikh 2008; Haken 2011; WWF/Dalberg 2012). There are no adequate estimates of the full scale of wildlife traded throughout the world given its diversity, scope and partial underground existence. Uncertainty surrounding this issue is enhanced by lack of international data standards and varying commitments to data collection infrastructure within and between countries.
Fundamental terms such as “legal” and “illegal,” “formal” and “informal” may be subjective and based upon which regulations are applied and the context of the trade (e.g., national laws vary by country for trade in a particular species, certain species can be traded for particular purposes but not for others). In some cases, legal trade is well recorded by border officials while in other cases it is largely ignored. Confiscated illegal trade is often reported but undetected illegal shipments regularly go unrecorded. Legality of wildlife trade in most instances does not correlate with disease risk posed, as the majority of wildlife trade regulations (e.g., the Convention on International Trade in Endangered Species of Wild Fauna and Flora; CITES) are in place to conserve certain species or regulate economies rather than protect health.
Although wildlife trade is often lumped into a single entity, this enterprise is comprised of a multitude of products such as food, trophies, pets, fashion, medicine, artifacts and aphrodisiacs. Within each category exist a range of specialty market value chains that vary in motivating economics, cultural and societal origins, geographic source and destination, transportation type and route, trader and consumer identities, behavioral practices, species volume and condition, local and international legality. This results in vastly variable threats including loss of biodiversity, invasive alien species, food security and emergence of both high- and low-consequence pathogens. Thus, threats can only be quantified in response to specific questions (i.e., examining unique traits of specific market chains/pathways).
Timber and plants are estimated to comprise nearly 70% of the known (broadly defined) wildlife global trade value, leaving non-aquaculture fisheries products responsible for 28% and ornamental fish, mammals, herpetofauna and other species responsible for roughly 2% (US $5.27 billion) (Engler and Parry-Jones 2007; Ahlenius 2008).
The majority of live wild animal trade is comprised of aquatic animals and herpetofauna traded mainly for the pet industry. China and Southeast Asian countries are the top global exporters, while the USA and European Union (EU) are the top importing consumers (Altherr et al. 2011) of aquatic and herpetofauna wildlife. A portion of this trade is recorded by weight only, leaving the total number of individual animals involved unquantified. Approximately 187 million live fish are imported to the USA annually, 92% of which are freshwater taxa (Smith et al. 2008). Live turtles and frogs are also commonly imported as pets as well as food items. The USA imports on average 2280 tons of frog legs in addition to 2216 tons of live frogs for consumption each year (Altherr et al. 2011).
Birds and mammals are also highly represented among a myriad of known global trade routes for exotic pets (Bush et al. 2014). A review of this trade found it to be an expanding, yet fluid and dynamic industry with reasons for its growth including human population expansion, increasing affluence in South America and East Asia (resulting in a larger market for exotic pets), use of the internet and a broadening interface with wildlife habitat (Bush et al. 2014).
Given global variability in laws and difficulty in distinguishing between legal and illegal transactions (e.g., false declarations of geographic origin, captive vs. wild-caught, misrepresentation of purpose of import or final destination), monitoring legality of wildlife trade is comparable in complexity to weapons trade. In the majority of instances, the legality of trade of wildlife at the international and national level is determined by authorities tasked with conservation rather than public or animal health protection. Specifically, unpermitted trade of CITES-listed species across international borders comprises the bulk of what is considered and/or reported as global illegal wildlife trade.
As with legal trade of wildlife, species are traded illegally as exotic pets, specialty foods, traditional medicines, trophies and fashion items. Drivers of this illicit trade vary from financial to cultural to relic.
Because the drivers and components of illegal wildlife trade are highly variable, the perpetrators do not fit any one category nor does their trade behavior follow a single pathway. Diverging networks include local village hunters, criminal groups engaged in drugs or terrorism, government officials and other economically driven sellers and consumers (Hayman and Brack 2002; Warchol et al. 2003; Wyler and Sheikh 2008; WWF/Dalberg 2012).
CITES maintains a database of reported trade of CITES-listed species only. The database is managed by the United Nations Environment Programme–World Conservation Management Center (UNEP–WCMC) and currently holds 7 million records of trade involving 50,000 scientific names of taxa listed by CITES. Currently, more than 500,000 trade records are reported annually (http://www.cites.org/eng/resources/trade.shtml).
There are also trade data held by the United Nations Statistics Division Comtrade. These data are maintained in broader categories such as “live animal” or “reptile skins.” Although some of these data are more specific, species level detailed information is generally not available (Chan et al. 2015). The Comtrade data are self-reported by trading partners, and as a result, there are inconsistencies and may also be variable reporting even within the broader categories.
Additionally, there are data held by national governments that vary widely in their format and scope, and rely largely upon efforts of authorities given national laws and priorities. These data are often not available to the public but some summaries may be found in gray literature reports. All importers of wildlife to the USA are mandated to submit a 3–177 (www.fws.gov/le/pdf/3177_1.pdf) request to the US Fish and Wildlife Service (USFWS) which in turn records details of the imports into the Law Enforcement Management Information System (LEMIS) database. This database includes both CITES and non-CITES species considered to be wildlife per the USFWS definition (50 CFR 14.4). This database therefore holds records of all declared wildlife imports to the USA and, theoretically, details of illegal imports confiscated by authorities at US ports of entry. Although some wildlife species are regulated by other US agencies such as the United States Department of Agriculture (USDA), Centers for Disease Control and Prevention (CDC), and Food and Drug Administration (FDA), imports of wildlife as defined by USFWS are also tracked in LEMIS despite this overlap in jurisdiction. Therefore, the LEMIS system represents a comprehensive data source for incoming wildlife to the USA (with few exceptions such as bushmeat items that are not determined to be of CITES origin). LEMIS data are maintained by USFWS for 5 years.