Summarizing US Wildlife Trade with an Eye Toward Assessing the Risk of Infectious Disease Introduction

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.

Since 2005, LEMIS data spanning January 1, 2000–August 6, 2013, have been collected, standardized, cleaned (e.g., misspellings) and entered into a propriety database structure curated by EcoHealth Alliance (EHA). The dataset, entitled “WILDb,” includes taxonomical, geographic and count information for each shipment that entered the USA and its territories, allowing for pathway analyses to be conducted on a global level for wildlife that entered the USA. The results presented here are a preliminary analysis of this comprehensive database of wildlife trade into the USA. The dataset continues to be periodically updated.

As of January 2015, WILDb included a total of 5,207,420 individually identifiable wildlife shipments entering the USA between January 1, 2000, and August 6, 2013. The number of annually declared wildlife shipments doubled during the period examined (Figure 1), reaching approximately 400,000 declared shipments imported in 2012.

These shipments included a total of 11,033,468,322 individual specimens/animals, plus an additional 977,109,143 kg of specimens/animals measured only in weight. Of these, 3,028,647,093 (27.4%) individuals plus 24,449,892 (2.5%) kg were recorded as live upon entry. Thus, for the period 2000–2012, there was an annual average of 224.9 million (s = 42.3 million; median = 231.5 million) live animals plus an additional 1.8 million kilograms of live animals imported into the USA as recorded in the LEMIS database.

We selected the top ten categories represented by the data for illustration of the most frequent wildlife taxa imported to the USA. The majority of wildlife shipments (by taxon) contained mammal products (most of which were non-live; Figure 2a), while the majority of total specimens imported were shells and tropical fish (Figure 2b). This is due to the fact that shipments of mammals and their products contain fewer individuals or items while large volumes of aquatic species can be transported in a single shipment.

Nearly one-third of all wildlife shipments entering the USA contained live animals, the vast majority of which were imported by the aquatic and pet industry. Aquatic, amphibian and invertebrate species accounted for approximately 50% of recorded shipments of live animals to the USA. Top specimens involved in such live shipments are represented in Figure 3. Once the aforementioned subset is removed, reptile, rodent and bird species destined for the exotic pet trade make up the majority of remaining live imports. While roughly 27% of incoming live wildlife shipments contained mammals, this taxon only represented 4% of overall number of specimens imported (approximately 406,662,421 individual mammals, plus additional mammals documented only by weight vs. number of animals). Excluding those recorded only by weight, 2,434,851 live mammals were imported.

The data contained reported both “country of origin” and “country of export.” This reporting is by the importer/exporter, and therefore, country of origin may be falsely reported without means for authorities to verify source. The stated origin of imported live wildlife from 2000 to 2013 was roughly 77.7% wild and 17.7% captive (4.6% listed as ranched or other). Since many species traded may be wild-caught or captive-raised, it remains difficult for authorities to identify false reporting of wild versus captive and true country of origin, despite visual inspection and means of import. The reported countries of origin from 2000 to 2013 for all declared US wildlife imports by shipment are shown in Figure 4, with Indonesia as the leading exporter. However, at the specimen level (i.e., number of individual animals/products imported), China was the leading exporter. Many imports were not identified at the species level.

China and Southeast Asia was a primary region of origin for US wildlife imports. The vast majority of both live and non-live wildlife imported from this area were aquatic, invertebrate and herpetofauna species. Indonesia was responsible for exporting the most live wildlife shipments to the USA during the period examined, comprised mainly of these aforementioned species. However, live mammals and birds were also imported. Examples of identified live species imported from China included over 120,000 kg of live American bullfrogs (Rana catesbiana)—a conservatively estimated 360,000 frogs—imported mainly for food, nearly 30 million live pheasants (Phasianus colchicus spp.), approximately 150,000 live macaques, in addition to live bats for research and Asiatic chipmunks for pets in fewer numbers. Vietnam was the exporter of 300 shipments of live macaques to the USA during the period examined. Taiwan exported approximately 450,000 finch-like live pet birds including canaries and goldfinches, and Indonesia exported over 85,000 kg of “edible-nest swiftlet” nests to the USA.

The primary origins of mammal imports specifically were Canada and South Africa based on number of shipments, and the USA and China for number of specimens/animals imported. More than 15,000 live bison were imported from Canada annually, and additional amounts recorded only by weight. Likewise hoofstock made up the majority of mammal imports from South Africa. Wildlife imports that were listed as having the USA as country of origin included deer, squirrel, bear, alligator, avian products and aquatic species such as squid.

Nearly half of all declared wildlife imports to the USA came through the ports of New York, Los Angeles and Miami (USFWS Regions 8, 5 and 4, respectively) (Figure 5).

Ninety-nine percent of recorded imports were legally declared. This percentage is a reflection of the vast amount of declared trade recorded dwarfing the number of confiscations at US borders. Commonly refused imports (shipments deemed illegally imported to the USA by USFWS or other US agency regulations and thus refused entry) included sturgeon (caviar), baby harp seal pelts, Indian peafowl (peacock) feathers, white tailed deer products such as antler, elephant ivory (e.g., décor, trophies, jewelry), sea turtle products (e.g., leather), crocodilians (e.g., leather), musk deer (traditional medicine products), and reptile and ostrich products (e.g., leather).

While most illegal shipments presented at the Mexican border, the majority of illegal specimens (number of animals) that presented at ports of entry originated in China. Such items included deer and bear medicinal items, macaque scientific specimens, live aquatic species and reptiles. Documented origins of illegally imported live wildlife to the USA by specimen are illustrated in Figure 6, with Indonesia as the leading country of origin. The most common of these live refused specimens were comprised of corals, fish and herpetofauna from Southeast Asia, as well as birds and corals from the Caribbean. The most common origins of live, non-aquatic confiscations (by specimen) included herpetofauna and bird species from Africa, Asia and South America.

As with all big data, there is uncertainty in this dataset. For example, non-CITES-listed species imports often lacked detail in several areas of the USFWS LEMIS database, suggesting such shipments were less scrutinized. Typically, “species” was recorded by USFWS using a four-letter “species code.” However, codes exist for several taxonomic levels (species, genus and more general “non-CITES” or “NA” descriptors), and a large portion of the data did not include species level identification. Further, codes often overlapped and/or several different codes were used to describe a single species. Currently, WILDb contains 14,074 unique species codes. EHA was able to ascertain some level of taxonomic information for over 98% of the data entries despite the fact that the majority of these did not provide specific species identification. This study was further limited to wildlife imports that were either accepted or rejected by authorities and did not include illegal shipments that evaded authorities as those go inherently unrecorded and unrecognized.

Given the sheer volume of live wildlife and wildlife product imports to the USA, and the fact that most refused shipments were due to CITES status and not based upon the risk of disease introduction, we believe it is prudent to further assess risk of pathogen introduction via wildlife trade. The current regulatory atmosphere for this goal is highly fragmented. The USFWS currently does not focus primarily on disease prevention, but on conservation status; the CDC currently focuses on specific health risks associated with non-human primates, African rodents and bats; and the USDA regulates non-domestic hoofstock, birds and few other specific mammals that originate in countries positive for reportable diseases. These species are regulated for specific diseases and thus may be approved entry if deemed safe.