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Abstract

The global trade in wildlife provides disease transmission mechanisms that not only result in human disease outbreaks, but also threaten livestock, international trade, rural livelihoods, native wildlife populations, and the health of ecosystems. Global movement of animals for the pet trade is estimated at some 350 million live animals, worth approximately US$20 billion per year. Approximately one-quarter of this trade is thought to be illegal, hence not inspected or tested. Disease outbreaks resulting from trade in wildlife 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 wildlife trade. Wild animals are captured, transported, and sold either live or dead and commingled throughout the process in a system of scale-free networks with major hubs rather than random or evenly distributed supply systems. As focal points for distribution and sales, the hubs provide control opportunities to maximize the effects of regulatory efforts as demonstrated with domestic animal trading systems (processing plants and wholesale and retail markets, for example). Focusing efforts at markets to regulate, reduce, or in some cases, eliminate the commercial trade in wildlife could provide a cost-effective approach to decrease the risks for disease in humans, domestic animals, wildlife, and ecosystems.
IMPLICATIONS OF WILDLIFE TRADE ON THE MOVEMENT OF AVIAN
INFLUENZA AND OTHER INFECTIOUS DISEASES
1,2
William B. Karesh,
3,5
Robert A. Cook,
3
Martin Gilbert,
3
and James Newcomb
4
1
Presentation at the FAO and OIE International Scientific Conference on Avian Influenza and Wild Birds, FAO, Rome,
30 and 31 May 2006.
3
Wildlife Conservation Society, 2300 Southern Blvd., Bronx, New York 10460, USA
4
Bio-Economic Research Associates, Boulder, Colorado 20302, USA
5
Corresponding author (email: wkaresh@wcs.org)
ABSTRACT:
The global trade in wildlife provides disease transmission mechanisms that not only
result in human disease outbreaks, but also threaten livestock, international trade, rural
livelihoods, native wildlife populations, and the health of ecosystems. Global movement of
animals for the pet trade is estimated at some 350 million live animals, worth approximately
US$20 billion per year. Approximately one-quarter of this trade is thought to be illegal, hence not
inspected or tested. Disease outbreaks resulting from trade in wildlife 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 wildlife trade. Wild animals are
captured, transported, and sold either live or dead and commingled throughout the process in
a system of scale-free networks with major hubs rather than random or evenly distributed supply
systems. As focal points for distribution and sales, the hubs provide control opportunities to
maximize the effects of regulatory efforts as demonstrated with domestic animal trading systems
(processing plants and wholesale and retail markets, for example). Focusing efforts at markets to
regulate, reduce, or in some cases, eliminate the commercial trade in wildlife could provide a cost-
effective approach to decrease the risks for disease in humans, domestic animals, wildlife, and
ecosystems.
Key words: Avian influenza, Ebola, infectious disease, networks, SARS, wildlife trade.
Threats to the health of people, animals,
and ecosystems, and the risk factors for
emerging infectious diseases run the
gamut from climate change to poverty to
security issues. Few are as immediately
manageable as the risk factor of global
trade in wildlife. Trade in wildlife provides
disease-transmission mechanisms at scales
that not only cause human disease out-
breaks but also threaten livestock, in-
ternational trade, rural livelihoods, native
wildlife populations, and the health of
ecosystems. Each year, roughly 350 mil-
lion live plants and wild animals are
shipped globally (World Wildlife Fund,
2001). Unfortunately, a single global total
is not available for wild animals alone and
much of the trade is illegal or not closely
monitored. Surveys of live wildlife in
markets in Guangzhou, China included
masked palm civets (Paguma larvata),
ferret badgers (Melogale spp.), barking
deer (Muntiacus reevesi), wild boar (Sus
scrofa), bamboo rats (Rhizomys sinensis),
endangered leopard cats (Prionailurus
bengalensis), and various species of hedge-
hogs, foxes, squirrels, gerbils, and snakes,
together with domestic dogs, cats, and
rabbits (Asia Animals Foundation, 2005).
Following the severe acute respiratory
syndrome (SARS) outbreak in 2003,
838,500 wild animals reportedly were
confiscated from the markets in Guangz-
hou (British Broadcasting Corporation,
2003). Daily, wild birds flow through
trading centers where they are in contact
with dozens of other species before being
shipped to other markets, sold locally, and
even freed back in the wild as part of
religious customs such as merit release
(Mather, 2005) or because they become
unwanted pets. In a single market in
North Sulawesi, Indonesia, up to 90,000
mammals are sold per year (Clayton and
2
Original presentation and current manuscript adapted
from: KARESH, W. B., R. A. COOK, E. L. BENNETT, and
J. NEWCOMB. 2005. Wildlife trade and global disease
emergence. Emerging Infectious Diseases 11: 1000–1002.
Journal of Wildlife Diseases, 43(3) Supplement 2007, pp. S55–S59
#
Wildlife Disease Association 2007
S55
Milner-Gulland, 2000). In a survey con-
ducted at one market in Thailand over 25
weekends, over 70,000 birds comprised of
276 species were sold (Round, 1990). In
lieu of precise trade data, we conserva-
tively estimate that in East and Southeast
Asia alone, tens of millions of wild animals
are shipped regionally and from around
the world annually for food or use in
traditional medicine. The estimate for
trade and local and regional consumption
of wild animal meat in Central Africa is
over one billion kilograms per year (Wilkie
and Carpenter, 1999) and estimates for
consumption in the Amazon Basin range
from 67 to 164 million kilograms annually
(Robinson and Redford, 1991; Peres,
2000). In Central Africa, the majority of
wild animals harvested are small mammals
(including small antelope and primates),
birds, and reptiles. Assuming an average
body weight of 5 kg results in a conserva-
tive estimate of 200 million animals in
Central Africa and 12–35 million in the
Amazon basin. The increasingly global
scope of this trade, coupled with rapid
modern transportation and the reality that
markets serve as network nodes rather
than as product endpoints (Dezso and
Barabasi, 2002), dramatically increases the
movement and potential cross-species
transmission of the infectious agents that
every animal naturally hosts. As with the
trade in domestic animals, the scale-free
network nature of the trade in wildlife also
provides opportunities for intervention
and control, as has been demonstrated
with foot and mouth disease, Newcastle’s
disease, and highly pathogenic avian in-
fluenza (HPAI).
Since 1980, over 35 new infectious
diseases, or about 1 every 8 mo, emerged
in humans (Smolinski et al., 2003). The
origin of human immunodeficiency virus
(HIV) is widely thought to be linked with
the human consumption of nonhuman
primates (Feng et al., 1999). Recent Ebola
hemorrhagic fever outbreaks in humans
were traced to index case contact with
infected great apes hunted for food (Leroy
et al., 2004). The severe acute respiratory
syndrome (SARS) coronavirus was associ-
ated with the international trade in small
carnivores and bats (Bell et al., 2004; Lau
et al., 2005) 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 (Tu et al.,
2004). The inadvertent movement of in-
fectious agents due to wildlife trade is not
limited to human pathogens but includes
those that can infect domestic animals as
well as native wildlife that serve as bi-
ological linchpins in environmental in-
tegrity. Highly pathogenic avian influenza
H5N1 virus was isolated from two moun-
tain hawk eagles (Spizaetus nipalensis)
illegally imported to Belgium from Thai-
land (World Organization for Animal
Health, 2004) as well as from passerines
shipped from east Asia to the United
Kingdom (Dudley, 2006). Newcastle’s
disease entered Italy via a shipment of
undetermined species of parrots, love-
birds, and finches imported from Pakistan
for the pet trade (World Parrot Trust,
2004). Monkeypox was introduced to
a native rodent species and subsequently
humans in the United States by importa-
tion of wild African rodents from Ghana
for the pet trade (Guarner et al., 2004).
Merit release of wild birds and reptiles
(the intentional release of animals as part
of religious or cultural practices) that have
passed through mixed animal markets
provides another avenue for introducing
novel infectious agents into the wild
(Karesh et al., 2005; Mather, 2005). This
warrants further investigation. Released
scaly-breasted munias (Lonchura punctu-
lata) along with other munia species tested
positive for HPAI H5N1 in Hong Kong in
2007 (Promed-Mail, 2007a). Also in 2007,
a black francolin (Francolinus francoli-
nus), a species commonly captured and
sold in markets as caged songbirds, tested
positive for HPAI H5N1 in Pakistan
(Promed-Mail, 2007b).
S56 JOURNAL OF WILDLIFE DISEASES, VOL. 43, NO. 3 SUPPLEMENT, JULY 2007
Many diseases are transmitted via para-
sites carried by imported animals. For
example, between November 1994 and
January 1995, U.S. Department of Agri-
culture personnel inspected 349 reptile
shipments from 22 countries containing
117,690 animals (U. S. Animal Health
Association, 1995). Ticks were removed
from animals in 97 shipments and infested
shipments included 54,376 animals (U. S.
Animal Health Association, 1995). Infor-
mation is not available to determine if the
above-mentioned ticks were tested for
pathogens; however, ticks carry many
diseases that threaten livestock and human
health, including heartwater disease,
Lyme disease, and babesiosis.
The threat of emerging infectious dis-
eases spreading among people and other
animals is rising, fueled by human activ-
ities ranging from the handling of bush-
meat and the trade in exotic animals to the
destruction of wild habitat (Walsh et al.,
1993; Lilley et al., 1997; Patz et al., 2000).
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 (Taylor et al., 2001).
Seventy-seven percent of pathogens found
in livestock are shared with other host
species (Haydon et al., 2002).
In addition to the direct health effects,
disease outbreaks destabilized trade, had
devastating effects on human livelihoods,
and caused hundreds of billions of dollars
of economic damage globally. The rash of
livestock disease outbreaks around the
world since the mid 1990s, including
bovine spongiform encephalopathy, foot
and mouth disease, avian influenza, and
swine fever are estimated to have cost
world economies over $80 billion (New-
comb, 2004). This figure does not include
the additional costs due to avian influenza
over the last 2 yr. In early 2003, the
United Nation’s Food and Agriculture
Organization reported that more than
two-thirds of global meat trade was
embargoed as a result of mad cow disease,
avian influenza, and other livestock dis-
ease outbreaks. Early efforts to control the
spread of HPAI H5N1 in Asian countries
included culling more than 140 million
chickens (World Health Organization,
2005), with considerable additional impact
since then. The projected growth of
industrial livestock production to meet
global protein demand in the coming
decades will increase the economic and
food security impacts of future disease
outbreaks.
Traditional approaches to reducing dis-
ease prevalence or exposure risks such as
culling or vaccination are not feasible for
the myriad of species around the world
included in the wildlife trade. Rather than
attempting to eradicate pathogens or to
eradicate the wild species that may harbor
them, a practical approach to decrease the
risk of spreading disease would include
decreasing the contact among species.
Closing retail poultry markets in Hong
Kong for just 1 day per month reduced
the rate of H9N2 avian influenza virus in
market birds (Kung et al., 2003). Wang et
al. (2006) demonstrated the presence of
HPAI H5N1 in cages used for marketing
live domestic poultry in Guangzhou,
China. Little equivalent work has been
conducted in market systems selling wild-
life, but an analogous approach to the
precautionary principle (Convention on
Biological Diversity, 1992) might be ap-
propriate for taking action prior to the
next outbreak or pandemic. Wild bird
markets appear to present the same risks,
ifnotmore,duetoalackofclear
regulations and monitoring in many coun-
tries around the world. Major hubs
associated with wildlife marketing provide
control opportunities to maximize the
impact of regulatory efforts (Dezso and
Barabasi, 2002). Control strategies based
at such hubs could include surveillance for
species and sanitary regulation compli-
ance, strengthening and enforcing disease-
control regulations, developing and im-
plementing quarantine procedures, and
creating mechanisms to shift costs of
KARESH ET AL.—WILDLIFE TRADE AND AVIAN INFLUENZA S57
controlling disease outbreaks from the
public to the animal suppliers or vendors.
Focusing efforts at markets to regulate,
reduce, or eliminate the trade in wildlife
could provide a cost-effective approach to
decrease the risks of disease for humans,
domestic animals, wildlife, and ecosys-
tems.
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KARESH ET AL.—WILDLIFE TRADE AND AVIAN INFLUENZA S59
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The SARS-CoV-2 pandemic has caused immense social and economic costs worldwide. Most experts endorse the view that the virus has a zoonotic origin with the final spillover being associated with wildlife trade. Besides human consumption, wild animals are also extensively traded as pets. Information on zoonotic diseases has been reported to reduce consumer demand for exotic pets. We conducted a global survey and collected 162 responses from international experts on exotic pet trade (traders, academics, NGOs, enforcement entities) to understand how the legal and illegal trade of exotic pets is expected to be affected by the ongoing coronavirus pandemic. Our results suggest that legal purchase of exotic pets is perceived as decreasing during the first pandemic wave due to: lower availability of animals for trade, suppliers’ inability to reach consumers and social distancing measures. The general perception is that in the future (i.e., next five years), both demand and supply of legally traded exotic pets are expected to either remain unchanged or decrease only temporarily. The consumer demand for illegal exotic pets is also expected to remain unchanged following the outbreak. The top two challenges reported by respondents, when considering the consequences of the pandemic for the exotic pet trade, are inadequate enforcement of national regulations and increased illegal trade. Our results suggest that the negative consequences of a zoonotic outbreak may not dissuade consumers of exotic pets. Worldwide, the transit/storing conditions and lack of health screenings of traded live animals are conducive to spreading diseases. Consumer demand is a key driver of trade, and enforcement of trade regulations will remain challenging, unless factors driving consumer demand are adequately incorporated in problem-solving frameworks. We emphasize the complexity of trade dynamics and the need to go beyond bans on wildlife trade. Stronger law enforcement, implemented along with initiatives dissuading consumption of wild exotic pets, are essential to sustainably satisfy the market demand.
... Human-animal interactions in wildlife trade practices create interfaces for pathogen spillover from their natural reservoirs to other animals and humans. Furthermore, disease can spread through the movement of animals over long distances from their natural habitats to densely populated human environments (Daszak et al. 2007;Karesh et al. 2007). Human activity in the wildlife trade has been identified as a risk factor for the emergence of severe acute respiratory syndrome (SARS) in 2002 and the re-emergence of highly pathogenic avian influenza (HPAI) in 2003 in China (Burgos and Burgos 2007;Field 2009;Peiris et al. 2004). ...
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Current wildlife trade practices in China lead to significant interactions between humans and animals and drive the emergence of zoonotic diseases. The at-risk behaviors, knowledge, and attitudes that influence health-related behaviors in relation to animal contact and safety measures in the trade remain poorly understood. A self-administered questionnaire survey was conducted among 947 adult Internet users in three provinces in southern China to assess knowledge, perceived disease risks, at-risk behaviors, and the association of these factors with other demographic factors among the target population. Few of the participants possessed sufficient knowledge of zoonotic diseases. Although most participants were opposed to the use of wild animal resources, many reported keeping wild animals as pets (30.7%) and eating wild animals (30.5%). The majority of participants (76.3%) believed the disease transmission via wildlife trade, but few connected contact with animals to sickness (18.5%) and only slightly more than half sought post-exposure treatment (54.4%). These results reveal low levels of knowledge and perceived risk regarding disease emergence from the animal–human interactions in wildlife trade and uncover the gaps in knowledge and attitudes as key challenges to the development of health behavior change interventions pertaining to wildlife trade.
... T he legal, international transport of undomesticated vertebrates as pets (hereafter, pet trade) is widespread and growing (Bush et al. 2014, Lockwood et al. 2019, involving billions of dollars in trade and millions of animals each year (Karesh et al. 2007, Bush et al. 2014. The pet trade is therefore a key economic resource, particularly for local traders that depend on it for their income (e.g., Raghavan et al. 2013, Robinson et al. 2018. ...
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The international trade in exotic vertebrate pets provides key social and economic benefits but also drives associated ecological, ethical, and human health impacts. However, despite its clear importance, we currently lack a full understanding of the structure of the pet trade, hampering efforts to optimize its benefits while mitigating its negative effects. In the present article, we represent and review the structure of the pet trade as a network composed of different market actors (nodes) and trade flows (links). We identify key data gaps in this network that, if filled, would enable network analyses to pinpoint targets for management. As a case study of how data-informed networks can realize this goal, we quantified spatial and temporal patterns in pets imported to the United States. Our framework and case study illustrate how network approaches can help to inform and manage the effects of the growing demand for exotic pets.
... While many human activities are known to influence the risk of zoonotic spill over (Allen et al. 2017;Gibb et al. 2020), wildlife trade has been identified as one of the major potential pathways of zoonotic disease emergence, as well as an activity that plays a role in maintaining endemic zoonotic diseases (i.e. those that regularly spill over from animals to humans) in circulation (Karesh et al. 2005;Karesh et al. 2007;Pavlin et al. 2009;Smith et al. 2012;OIE 2020). The scale of the global wildlife trade is difficult to quantify, with the nature of transactions varying from informal and highly localised markets to well established international trade routes that cover both legal and illegal shipments. ...
Technical Report
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Zoonoses represent a major global health challenge. They are responsible for billions of cases of human illness and millions of deaths each year, and the fallout from zoonotic diseases has the potential to have profound economic and social impacts on human society. In this context, wildlife trade has been identified as one of the important potential pathways of zoonotic disease emergence, as well as an activity that plays a role in maintaining existing zoonoses in circulation. In this report, we systematically reviewed literature detailing known associations between animals and zoonotic diseases to collate a dataset of 1,608 unique taxa associated with 369 pathogens causing 275 diseases. We then investigated the prevalence in trade over a ten- year period of CITES-listed taxa that have been associated with at least one zoonotic disease in this dataset, looking at the commodities that are traded as well as the key trade routes. We particularly concentrated on trade in live animals and meat, as two of the commodities that have been identified as having particularly high zoonotic risk. We also focussed our efforts on investigating trade at the family level, in order to address the issue of species sampling bias and because species within the same family are likely to carry similar zoonotic diseases.
... Like other taxa, reptiles can be reservoirs of a wide variety of pathogens, some of which may be of public health concern, particularly to immunocompromised individuals 82 . Due to the poorly regulated globalised trade in animals, diseases are increasingly spreading, with unfamiliar pathogens posing threats locally 83,84,85 . The emergence of new strains and potential 'host-jumping' of existing pathogens can also cause population die-offs and further threaten the survival of wildlife and captive populations not yet adapted to these novel diseases 86,87 . ...
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In the midst of a global biodiversity crisis, Hong Kong authorities seized a record-breaking 649 metric tonnes (MT) of rare and endangered wildlife across 1,404 seizures in 2018 and 2019. This report summarises Hong Kong’s growing wildlife seizures (2018-2019), prosecutions (2017-2020) and the city’s continuing role in the global illicit wildlife trade. Volumes seized in 2018 and 2019 surpassed all annual totals for the preceding decade (excluding 2015). Figures indicate a shift in trade dynamics with ivory in decline, pangolins (a staple of Hong Kong traffickers) remaining at devastatingly high levels and a worrying diversification of other endangered species in trade.
... Providing animals to pet stores is one of the legal activities associated with the wildlife trade (Auliya et al., 2016;Bush, Baker, & Macdonald, 2014;Maceda-Veiga, Domínguez-Domínguez, Escribano-Alacid, & Lyons, 2016;Ribeiro et al., 2019). Although most pet animals are procured legally, an estimated 25% of the global pet trade is illegal (Karesh, Cook, Gilbert, & Newcomb, 2007). Among the numerous animals involved in the global pet market, the contribution of fish is significant (Maceda-Veiga et al., 2016;Prakash et al., 2017;Raghavan et al., 2013). ...
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This situation analysis presents a thorough, evidence-based examination of the relationship between wildlife and zoonosis, wildlife and emerging human pathogens and associated diseases, their origins, drivers, and risk factors. There is considerable divergence of opinion around the subject both within and outside the biodiversity conservation community and given the ontological challenges and highly different perspectives, contradictory narrative is unsurprising. Context is all-important and to clarify this in the analysis, the evidence of human diseases coming from wildlife is compared to diseases emerging from domestic animals and humans themselves, to provide context and proportions of the relative risk. The report highlights key knowledge, and provides perspective on where research, policy, interventions, and capacity building are needed to reduce risks of zoonoses and emergent animal-origin human diseases globally.
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Several human and animal Ebola outbreaks have occurred over the past 4 years in Gabon and the Republic of Congo. The human outbreaks consisted of multiple simultaneous epidemics caused by different viral strains, and each epidemic resulted from the handling of a distinct gorilla, chimpanzee, or duiker carcass. These animal populations declined markedly during human Ebola outbreaks, apparently as a result of Ebola infection. Recovered carcasses were infected by a variety of Ebola strains, suggesting that Ebola outbreaks in great apes result from multiple virus introductions from the natural host. Surveillance of animal mortality may help to predict and prevent human Ebola outbreaks.
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During May and June 2003, the first cluster of human monkeypox cases in the United States was reported. Most patients with this febrile vesicular rash illness presumably acquired the infection from prairie dogs. Monkeypox virus was demonstrated by using polymerase chain reaction in two prairie dogs in which pathologic studies showed necrotizing bronchopneumonia, conjunctivitis, and tongue ulceration. Immunohistochemical assays for orthopoxviruses demonstrated abundant viral antigens in surface epithelial cells of lesions in conjunctiva and tongue, with less amounts in adjacent macrophages, fibroblasts, and connective tissues. Viral antigens in the lung were abundant in bronchial epithelial cells, macrophages, and fibroblasts. Virus isolation and electron microscopy demonstrated active viral replication in lungs and tongue. These findings indicate that both respiratory and direct mucocutaneous exposures are potentially important routes of transmission of monkeypox virus between rodents and to humans. Prairie dogs offer insights into transmission, pathogenesis, and new vaccine and treatment trials because they are susceptible to severe monkeypox infection.
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The search for animal host origins of severe acute respiratory syndrome (SARS) coronavirus has so far remained focused on wildlife markets, restaurants and farms within China. A significant proportion of this wildlife enters China through an expanding regional network of illegal, international wildlife trade. We present the case for extending the search for ancestral coronaviruses and their hosts across international borders into countries such as Vietnam and Lao People's Democratic Republic, where the same guilds of species are found on sale in similar wildlife markets or food outlets. The three species that have so far been implicated, a viverrid, a mustelid and a canid, are part of a large suite of small carnivores distributed across this region currently overexploited by this international wildlife trade. A major lesson from SARS is that the underlying roots of newly emergent zoonotic diseases may lie in the parallel biodiversity crisis of massive species loss as a result of overexploitation of wild animal populations and the destruction of their natural habitats by increasing human populations. To address these dual threats to the long-term future of biodiversity, including man, requires a less anthropocentric and more interdisciplinary approach to problems that require the combined research expertise of ecologists, conservation biologists, veterinarians, epidemiologists, virologists, as well as human health professionals.
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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.
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