Volume 11, Number 7—July 2005
Wildlife Trade and Global Disease Emergence
The global trade in wildlife provides disease transmission mechanisms that not only cause human disease outbreaks but also threaten livestock, international trade, rural livelihoods, native wildlife populations, and the health of ecosystems. Outbreaks resulting from wildlife trade have caused hundreds of billions of dollars of economic damage globally. Rather than attempting to eradicate pathogens or the wild species that may harbor them, a practical approach would include decreasing the contact rate among species, including humans, at the interface created by the wildlife trade. Since wildlife marketing functions as a system of scale-free networks with major hubs, these points provide control opportunities to maximize the effects of regulatory efforts.
Threats to global health and risk factors for emerging infectious diseases run the gamut from climate change to poverty to security issues, but few are as immediately manageable as the global trade in wildlife. Trade in wildlife provides disease transmission mechanisms at levels that not only cause human disease outbreaks but also threaten livestock, international trade, rural livelihoods, native wildlife populations, and the health of ecosystems. Quantifying the global wildlife trade is almost impossible since it ranges in scale from local barter to major international routes, and much is conducted illegally or through informal networks. Some estimates indicate that ≈40,000 live primates, 4 million live birds, 640,000 live reptiles, and 350 million live tropical fish are traded globally each year (1). Live wildlife in markets in Guangzhou, China, trade in masked palm civets, ferret badgers, barking deer, wild boars, hedgehogs, foxes, squirrels, bamboo rats, gerbils, various species of snakes, and endangered leopard cats, along with domestic dogs, cats, and rabbits (2). After the outbreak of severe acute respiratory syndrome (SARS) in 2003, 838,500 wild animals were reportedly confiscated from the markets in Guangzhou (3). Wild mammals, birds, and reptiles flow daily through trading centers, where they are in contact with persons and with dozens of other species before they are shipped to other markets, sold locally, or even freed and sent back into the wild as part of religious customs such as merit release (4) or because they become unwanted pets. In a single market in North Sulawesi, Indonesia, up to 90,000 mammals are sold per year (5). In a survey conducted at 1 market in Thailand for 25 weekends, >70,000 birds, representing of 276 species, were sold (6). A similar survey of 4 markets in Bangkok in 2001 found that of 36,537 observed birds; only 37% were native to Thailand, while 63% were nonnative species (7).
In lieu of precise trade data, we conservatively estimated that in East and Southeast Asia, tens of millions of wild animals are shipped each year regionally and from around the world for food or use in traditional medicine. The estimate for trade and local and regional consumption of wild animal meat in Central Africa alone is >1 billion kg per year (8), and estimates for consumption in the Amazon Basin range from 67 to 164 million kilograms annually (9,10); for mammals alone, this consumption consists of 6.4 million to 15.8 million individual animals (11). In Central Africa, estimates of the number of animals consumed by humans annually vary, but 579 million has been proposed (12).
Hunters, middle marketers, and consumers experience some type of contact as each animal is traded. Other wildlife in the trade is temporarily exposed, and domestic animals and wild scavengers in villages and market areas consume the remnants and wastes from the traded and potentially traded wildlife. These numbers combined suggest that at least some multiple of 1 billion direct and indirect contacts among wildlife, humans, and domestic animals result from the wildlife trade annually. The increasingly global scope of this trade, coupled with rapid modern transportation and the fact that markets serve as network hubs rather than as product endpoints, dramatically increases the movement and potential cross-species transmission of the infectious agents that every animal naturally hosts.
Since 1980, >35 new infectious diseases have emerged in humans (13), ≈1 every 8 months. The origin of HIV is likely linked to human consumption of nonhuman primates (14). Recent Ebola hemorrhagic fever outbreaks in humans have been traced to index patient contact with infected great apes that are hunted for food (15). SARS-associated coronavirus has been associated with the international trade in small carnivores (16), and a study comparing antibody evidence of exposure to this coronavirus demonstrated a dramatic rise from low or zero prevalence of civets at farms to an approximately 80% prevalence in civets tested in markets (17).
The inadvertent movement of infectious agents due to the wildlife trade is not limited to human pathogens but also affects pathogens of domestic animals and native wildlife. H5N1 type A influenza virus was recently isolated from 2 mountain hawk eagles illegally imported to Belgium from Thailand (18). A paramyxovirus highly pathogenic for domestic poultry entered Italy through a shipment of parrots, lovebirds, and finches imported from Pakistan for the pet trade (19). Monkeypox was introduced to a native rodent species and subsequently to humans in the United States by importing wild African rodents from Ghana for the US pet trade (20). Chytridiomycosis, a fungal disease now identified as a major cause of the extinction of 30% of amphibian species worldwide, has been spread by the international trade in African clawed frogs (21). Merit release of wild birds and reptiles that have passed through markets provides another avenue for introducing novel infectious agents into the wild (4) and warrants further attention (Figure).
Many diseases are transmitted through the same species of parasites carried by imported animals. For example, from November 1994 to January 1995, US Department of Agriculture personnel inspected 349 reptile shipments from 22 countries containing 117,690 animals. Ticks were removed from animals in 97 shipments, and infested shipments included 54,376 animals (22). Ticks carry many diseases that threaten livestock and human health, including heartwater disease, Lyme disease, and babesiosis.
The possibility of emerging infectious diseases spreading between persons and animals is rising, fueled by human activities ranging from the handling of bushmeat and the trade in exotic animals to the destruction or disturbance of wild habitat (23–25). In a list of 1,415 human pathogens, 61% are known to be zoonotic, and multiple host pathogens are twice as likely to be associated with an emerging infectious disease of humans (26). Seventy seven percent of pathogens found in livestock are shared with other host species (27).
In addition to the direct health effects of the pathogens on persons and animals, animal-related disease outbreaks have caused hundreds of billions of dollars of economic damage globally, destabilizing trade and producing devastating effects on human livelihoods. The rash of emerging or reemerging livestock disease outbreaks around the world since the mid 1990s, including bovine spongiform encephalopathy, foot-and-mouth disease, avian influenza, swine fever, and other diseases, has cost the world's economies $80 billion (28). In early 2003, the United Nation's Food and Agriculture Organization reported that more than one third of the global meat trade was embargoed as a result of mad cow disease, avian influenza, and other livestock disease outbreaks. Efforts to control the spread of avian influenza in Asian countries since 2003 have required the culling of >140 million chickens (29). The projected growth of industrial livestock production in nonindustrialized countries to meet global protein demand will increase the impact of future disease outbreaks on economic and food supply security. Some of these outbreaks will inevitably be linked to the trade in wildlife.
Rather than attempting to eradicate pathogens or the wild species that may harbor them, a practical approach to decrease the risk for the spread of infectious diseases would include decreasing contact among species. Closing down retail poultry markets in Hong Kong for 1 day per month reduced the rate of H9N2 avian influenza virus in market birds (30). Little equivalent research has been conducted in market systems that sell wildlife, but an analogous approach to the precautionary principle (31) would be an appropriate action to take before the next outbreak or pandemic. Since wildlife markets are a system of networks with major hubs, these trading points provide practical control opportunities to maximize the effects of regulatory efforts (32). Focusing efforts at markets to regulate, reduce, or in some cases, eliminate the trade in wildlife could provide a cost-effective approach to decrease the risks for disease for humans, domestic animals, wildlife, and ecosystems.
Dr. Karesh is the director of the Wildlife Conservation Society's Field Veterinary Program and also serves as the co-chair of the World Conservation Union Veterinary Specialist Group. His projects and programs focus on the links between wildlife, domestic animals, and human health and well-being in nonindustrialized countries around the world.
- World Wildlife Fund—United Kingdom. Souvenir alert highlights deadly trade in endangered species. [cited 2001 Sep 19]. Available from http://www.wwf.org.uk/news/scotland/n_0000000409.asp
- Asia Animals Foundation. Species list. [cited 2005 Feb 7]. Available from https://www.animalsasia.org/index.php?module=6&menupos=2&submenupos=5&lg=en
- British Broadcasting Corporation. Animals suffer in the war on SARS. [cited 2003 Apr 30]. Available from http://news.bbc.co.uk/1/low/world/asia-pacific/2989479.stm
- Mather R. Turtle release…Merit making and how to make it right! [cited 2005 Feb 7]. Available from http://www.tatnews.org/others/2250.asp
- Clayton LM, Milner-Gulland EJ. The trade in wildlife in North Sulawesi, Indonesia. In: Robinson JG, Bennett, EL editors. Hunting for sustainability in tropical forests. New York: Columbia University Press; 2000. p. 473–98.
- Round PD. Bangkok Bird Club survey of the bird and mammal trade in the Bangkok weekend market. Nat Hist Bull Siam Soc. 1990;38:1–43.
- Round PD, Jukmongkkol R. A survey of the bird trade in and around the Bangkok weekend market. Bangkok: Bird Conservation Society of Thailand and WWF International Programme, Thailand; 2003. p. 86.
- Wilkie DS, Carpenter JF. Bushmeat hunting in the Congo Basin: an assessment of impacts and options for mitigation. Biodivers Conserv. 1999;8:927–55.
- Robinson JG, Redford KH. Neo-tropical wildlife use and conservation. Chicago: University of Chicago Press; 1991.
- Peres CA. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. In: Robinson JG, Bennett EL, editors. Hunting for sustainability in tropical forests. New York: Columbia University Press; 2000. p. 168–98.
- Peres CA. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. Conserv Biol. 2000;14:240–53.
- Fa JE, Peres CA. Game vertebrate extraction in African and Neotropical forests: an intercontinental comparison. In: Reynolds JD, Mace GM, Redford KH, Robinson JG, editors. Conservation of exploited species. Cambridge: Cambridge University Press; 2003. p. 203–241.
- Institute of Medicine. Microbial threats to health: emergence, detection, and response 2003. Washington: National Academy Press; 2003.
- Feng G, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999;397:436–41.
- Leroy EM, Rouquet P, Formenty P, Souquière S, Kilbourne A, Froment J-M, Multiple Ebola virus transmission events and rapid decline of Central African wildlife. Science. 2004;303:387–90.
- Bell D, Roberton S, Hunter PR. Animal origins of SARS coronavirus: possible links with the international trade in small carnivores. Philos Trans R Soc Lond B Biol Sci. 2004;359:1107–14.
- Tu C, Crameri G, Kong X, Chen J, Sun Y, Yu M, Antibodies to SARS coronavirus in civets. Emerg Infect Dis. 2004;10:2244–8.
- Van Borm S, Thomas I, Hanquet G, Lambrecht B, Boschmans M, Dupont G, Highly pathogenic H5N1 influenza virus in smuggled eagles, Belgium. Emerg Infect Dis. 2005;11:702–5.
- World Parrot Trust. Deadly Newcastle disease discovered in parrots and other birds imported from Pakistan to Italy. [cited 2004 Feb 29]. Available from http://www.worldparrottrust.org/news/end/pr29feb2004.htm
- Guarner J, Johnson BJ, Paddock CD, Shieh W-J, Goldsmith CS, Reynolds MG, Monkeypox transmission and pathogenesis in prairie dogs. Emerg Infect Dis. 2004;10:426–31.
- Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R. Origin of the amphibian chytrid fungus. Emerg Infect Dis. 2004;10:2100–5.
- Proceedings of the ninety-ninth annual meeting of the U.S. Animal Health Association. Richmond (VA): U.S. Animal Health Association; 1995.
- Lilley B, Lammie P, Dickerson J, Eberhard M. An increase in hookworm infection temporally associated with ecologic change. Emerg Infect Dis. 1997;3:391–3.
- Patz JA, Graczyk TK, Geller N, Vittor AY. Effects of environmental change on emerging parasitic diseases. Int J Parasitol. 2000;30:1395–405.
- Walsh JF, Molyneux DH, Birley MH. Deforestation: effects on vector-borne disease. Parasitology. 1993;106(Suppl):S55–75.
- Taylor LH, Latham SM, Woolhouse MEJ. Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci. 2001;356:983–9.
- Haydon DT, Cleaveland S, Taylor LH, Laurneson MK. Identifying reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis. 2002;8:1468–73.
- Newcomb J. Biology and borders: SARS and the new economics of bio-security, [cited 2004 February 7]. Available from: http://www.bio-era.net
- World Health Organization. Avian influenza: assessing the pandemic threat. WHO/CDS/2005.29. Geneva: The Organization; 2005.
- Kung NY, Guan Y, Perkins NR, Bissett L, Ellis T, Sims L, The impact of a monthly rest day on avian influenza virus isolation rates in retail live poultry markets in Hong Kong. Avian Dis. 2003;47:1037–41.
- Convention on Biological Diversity. Jakarta mandate, 1992. Available from http://www.biodiv.org/programmes/areas/marine/precautionary.aspx
- Dezso Z, Barabasi A. Halting viruses in scale-free networks. [R]. Phys Rev E Stat Nonlin Soft Matter Phys. 2002;65:055103.
Suggested citation for this article: Karesh WB, Cook RA, Bennett EL, Newcomb J. Wildlife trade and global disease emergence. Emerg Infect Dis [serial on the Internet]. 2005 Jul [date cited]. http://dx.doi.org/10.3201/eid1107.050194