Download Primates on display: Potential disease consequences beyond

Received: 2 June 2016
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Revised: 17 November 2016
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Accepted: 18 November 2016
DOI 10.1002/ajpa.23145
AJPA YEARBOOK ARTICLE
Primates on display: Potential disease consequences beyond
bushmeat
Michael P. Muehlenbein
Department of Anthropology, University of
Texas at San Antonio
Correspondence
Department of Anthropology, University of
Texas at San Antonio, One UTSA Circle,
MH 4.3.44, San Antonio, Texas 78249.
Email: [email protected]
Abstract
Human interactions with nonhuman primates vary tremendously, from daily cultural engagements
and food commodities, to pet ownership and tourist encounters. These interactions provide
opportunities for the exchange of pathogenic organisms (both zoonoses and anthroponoses). As
exposures are not limited to areas where bushmeat usage continues to be a major problem, we
must work to understand better our motivations for engaging in activities like owning primates as
pets and having direct physical contact with wild primates within the context of nature-based
tourism. These topics, and the theoretical potential for pathogen transmission, are reviewed in the
present manuscript. This is followed by a case study utilizing 3845 survey responses collected
from four international locations known for primate-based tourism, with results indicating that
while a majority of people understand that they can give/get diseases to/from wild primates, a surprising percentage would still touch or feed these animals if given the opportunity. Many people
still choose to touch and/or own primates, as their drive to bond with animals outweighs some
basic health behaviors. Desires to tame, control, or otherwise establish emotional connections
with other species, combined with the central role of touch for exploring our environment, necessitate the development of better communication and educational campaigns to minimize risks of
emerging infectious diseases.
KEYWORDS
anthroponoses, biophilia, bushmeat, companion animals, ecotourism, emerging infectious diseases,
environmental attitudes, haptics, Monkeyland Primate Sanctuary, primates, pets, Saint Kitts, Sepilok Orangutan Rehabilitation Centre, Takasakiyama Monkey Park, zoonoses, zoos
1 | INTRODUCTION
may be, our species has been dependent upon other species for survival, and understanding the range of emotional responses we have
Contextualizing our relationships and interactions with nonhuman ani-
toward these species is important for determining any risks associated
mals (referred to as animals from this point forward) is critical for
with human–animal interactions. One of the most critical risks of these
understanding our place in nature. For many people, feeling like a part
interactions is the potential for infectious disease outbreaks (see
of the natural world has always been, and will continue to be, a normal
Muehlenbein, 2016 for a detailed review).
state of being (Leopold, 1949). For those of us, we are captivated by
Pathogens are infectious organisms that parasitize other host
the natural world (Fromm, 1964), and this “biophilia” according to some
organisms, resulting in host illness (disease). There are at least 1415 of
scholars may include innate tendencies to emotionally affiliate with
these found in humans (Taylor, Latham, & Woolhouse, 2001), and com-
other living organisms (Kellert & Wilson, 1993; Wilson, 1984). For
bined they accounted for approximately seventeen percent of all global
other people, the commodification of nature provides a simple source
deaths in 2012 (World Health Organization, 2016). Many of these
of food, shelter, medicine, and other products, although people’s atti-
pathogens are considered emerging infectious diseases (EIDs) that are
tudes about the environment appear to have changed over the past
newly identified or evolved, or moved into new geographic areas or
several decades, particularly in developed populations (the New Envi-
new host populations (Lederberg, Shope, & Oakes, 1992). Zoonotic dis-
ronmental Paradigm: Dunlap & Van Liere, 1978). Whatever the case
eases (those originating from animals) are common, accounting for
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sixty-one percent of all known human pathogens and seventy-five per-
(Calattini et al., 2006; Calvignac-Spencer et al., 2012; Filippone et al.,
cent of all EIDs (Taylor et al., 2001).
2015; Kazanji et al., 2015; Vandamme, Salemi, & Desmyter, 1998;
The present manuscript aims to contextualize the potential risks of
Wolfe et al., 2005; Zheng et al., 2010) and simian foamy viruses
pathogen transmission between humans and nonhuman primates
me
et al., 2010, 2012; Mouinga-Onde
me
& Kazanji,
(Mouinga-Onde
(referred to as primates from this point forward). Given our phyloge-
2013; Switzer et al., 2008, 2012; Wolfe, Prosser, et al., 2004; Wolfe,
netic relatedness, we are susceptible to many different zoonoses from
Sreevatsan, et al., 2004). And human immunodeficiency viruses origi-
primates, and primates can be very susceptible to our anthroponoses
nated from primate bushmeat in West Africa (Ayouba et al., 2013; Gao
(reverse zoonoses) (Davies & Pedersen, 2008; Muehlenbein, 2016). We
et al., 1992, 1999; Hirsch, Olmsted, Murphey-Corb, Purcell, & Johnson,
share susceptibility to many pathogens like Ebola virus (Formenty,
1989; Huet, Cheynier, Meyerhans, Roelants, & Wain-Hobson, 1990;
Boesch, & Wyers, 1999), influenza (Karlsson, Engel, Feeroz, & San,
Keele et al., 2006; Plantier et al., 2009; Van Heuverswyn et al., 2006;
2012), and tuberculosis (Mycobacterium spp.) (Wolf, Sreevatsan, Travis,
Yamaguchi, Devare, & Brennan, 2000). In general, markets selling wild-
Mugisha, & Singer, 2013). This shared susceptibility has been of intense
life are particularly prone to facilitating the emergence of zoonotic
historical interest (Brack, 1987), and documenting these pathogen
pathogens (Greatorex et al., 2016), and this infected primate bushmeat
exchanges is important for predicting outbreaks in human populations
is even being shipped worldwide (Smith et al., 2012; Temmam et al.,
as well as the potential negative impacts we can have on many endan-
2016).
gered primate populations. For example, wild primates serve as reservoirs for a variety of malaria species that can infect humans (Baird,
2 | BEYOND BUSHMEAT
2009; Galinski & Barnwell, 2009; Singh et al., 2004), and human
tuberculosis (Mycobacterium tuberculosis) and herpes simplex virus
In addition to consumption and shared (sympatric) habitat overlap, ani-
can spread rapidly and be deadly in some primate populations
mal exhibitions (including tourism) and companion animals (pets) pres-
(Mätz-Rensing et al., 2015; Schrenzel, Osborn, Shima, Klieforth, &
ent complex and abundant opportunities for pathogen transmission.
Maalouf, 2003).
The following review attempts to summarize what is known about the
PubMed and Google Scholar were recently (November 2016)
potential of pathogen transmission within these contexts, in particular
searched by the author using terms “primate” and “zoono*” to identify
the human attitudes and behaviors that place ourselves and other spe-
papers reporting suspected and confirmed instances of pathogen trans-
cies at risk. The desire to tame or control other species appears central
mission between humans and wild populations of primates. Eliminating
to our own species (Shipman, 2010). While there has always been and
cases of pathogens exchanged in zoos, sanctuaries, clinics, laboratories,
still remains significant cultural variation in how animals are treated and
and other facilities, a minimum of sixteen different pathogenic organ-
for what purposes they have been either bred or controlled (Gray &
isms are confirmed (using genetic, serological, and/or microbiological
Young, 2011; Hurn, 2012), viewing animals on exhibit has a long his-
techniques) to have been transmitted from wild primates to humans
tory. This includes private animal collections, circuses, animal fighting,
(M. Muehlenbein, in preparation). These include simian foamy viruses,
baiting, trophy hunting, racing, rodeos, bullfighting, and similar encoun-
malaria, immunodeficiency viruses, and T-lymphotropic viruses, among
ters, and of course permanent institutions like zoos and aquariums. Pri-
others. Eight pathogenic organisms are confirmed to have been trans-
mates play a central role in these facilities and activities. Many people
mitted from humans to wild primates, and many of these have had dev-
live with wild primates as part of their daily lives. Primates play central
astating effects on ape populations, such as human metapneumovirus
roles in a number of religious traditions, most prominent being the
in gorillas and chimpanzees (Kaur et al., 2008; Palacios et al., 2011).
Howler Monkey God (Mayan Classic period), Sun Wukong (Chinese
Several of these organisms have been transmitted between the popula-
mythological Monkey King), Sarutahiko (Shinto monkey-like God of
tions on multiple occasions, and many other organisms are suspected
Crossroads), and Lord Hanuman (Hindu god of the epics Ramayana and
to have been transmitted, but lack appropriate laboratory confirmation.
Mahabharata). Primates represent important commodities in some cul-
The true numbers of zoonoses and anthroponoses involving wild pri-
tures (Fuentes, 2013), and many of these animals are kept for utilitarian
mates are probably much higher.
purposes, like pigtailed macaques (Macaca nemetrina) for picking coco-
Arguably the majority of attention on primate-related zoonoses
nuts in Thailand (Sponsel, Ruttanadakul, & Natadecha-Sponsel, 2002).
has focused on the acquisition of pathogens via the hunting, prepara-
To others of us who do not have primates as part of our daily lives,
tion, and consumption of wild animals (bushmeat). For many, many
encounters with them may seem exotic. Primates exhibit social cogni-
people, wild primates are hunted and sold for household income, or
tive abilities greater than most other species. As frugivores and foli-
consumed as an important source of protein (Covey & McGraw, 2014).
vores (primarily), they seem approachable to us, particularly as they are
Primate bushmeat is often preferred over some other species by differ-
portrayed in the media as jovial and neotenous. Some people may per-
ent people in different areas (Fa, Juste, Burn, & Broad, 2002). Particu-
ceive their risks of injury as relatively low when interacting with non-
larly in West and Central Africa, primate bushmeat has been a source
carnivores; not accounting for contagious illnesses, most injuries are
of a number of pathogen outbreaks, including Ebola virus disease
perceived to be minor (e.g., small scratches and bites).
(Muyembe-Tamfum et al., 2012). Exposure to primate fluids via hunting
In general, people tend to develop an affinity for cute and furry ani-
and butchering has led to the transmission of T-lymphotropic viruses
mals; they fulfill the Japanese cultural concept of “kawaii” (quality of
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cuteness) without requiring much anthropomorphizing. For the most
engagement with these animals in our homes (as pets), at animal-based
part, primates, particularly young animals, are beautiful creatures that
entertainment facilities (e.g., zoos), and in the wild through nature-
may stimulate the human desire to touch. As a species, we have an
based tourism.
innate urge to explore our environment through touch. There are a
number of lines of evidence to support such a conclusion, from the
3 | ANIMALS IN THE HOME
roles of grooming and embracing in primates to form and maintain
social relationships and coalitionary support, reconciling when disagree-
When one loves animals and children too much, one loves them
ments happen, to the pervasiveness of stuffed animals in many cul-
against human beings (Sartre, 1981, p. 30)
tures, and the almost autonomic urges to touch even taxidermy
Worldwide, a majority of people seek companionship with some
specimens (Milgrom, 2010). It is long known that physical contact is an
type of animal in their home (Serpell, 1986), and this began with the
important part of normal development in many species (Harlow, 1958).
et al.,
domestication of dogs as early as 32,000 year ago (Germonpre
Touch is so important that we must put signs throughout zoos and
2009). As “pets,” these animals are named, intentionally bred, and usu-
museums (and even on working dogs!) to remind us not to handle the
ally allowed in the home (yet they are still castrated/neutered and oth-
animals or exhibits, and touch even remains an important part of the
erwise physically altered). Many of us celebrate their birthdays and
shopping experience, despite widespread adoption of online purchasing
take them on vacation with us. The American Pet Products Association
(Peck & Childers, 2003).
recorded more than $60 billion in industry expenditures in 2015, with
Touch certainly preceded language as a form of communication in
most on food, supplies, and veterinary care (American Pet Products
our own species. We use our skin to express intimate emotional state,
Association, 2016). Sixty-five percent of US households own a pet,
and external manifestation of affect dependent upon type, duration,
with more than 77 million dogs and 85 million cats (American Pet Prod-
frequency, intensity, and area of touch (Hertenstein, Verkamp, Ker-
ucts Association, 2016).
estes, & Holmes, 2006). There is a rich literature on “haptics” (Gibson,
There are various benefits to companion animal ownership. For
1966), the somatosensory system of identifying and communicating
example, pet ownership, particularly that of dogs, is associated with
tactile information and the associated physiology of mechanical stimu-
increased physical activity (Cherniack & Cherniack, 2015). As adults,
lation and correlated neurological processes (Gordon et al., 2013;
those who experienced responsibility for pets as a child may be primed
Lederman & Klatzky, 2009; Vrontou, Wong, Rau, Koerber, & Anderson,
to express greater concern for wildlife and more compassion for other
2013). Touch is used as an important therapeutic intervention to
people as adults (Paul & Serpe, 1993). Having responsibility for a pet as
improve a variety of health outcomes (Bush, 2001). Animal-assisted
a child even exposes children to the concept of death when the animal
therapy is associated positively with moderate improvements in autism
, 2006). Our desire to care for and support other
perishes (Dupre
spectrum symptoms (Nimer & Lundahl, 2007) and other behavioral and
dependent species is illustrated by examples ranging from the popular-
medical outcomes, including reduced anxiety (Barker & Dawson, 1998).
ity of virtual pet products (e.g., Tamagotchi, Petz, Anipalz, and Ninten-
In places where animal presence may be prohibited, like care facilities
dogs), to the practice of women of the Yanomami of Venezuela and
for the immunocompromised and other special needs individuals,
Brazil, the Huaorani of Ecuador, and the Guaj
a of Brazil breastfeeding
robotic companions may allow for important tactile interactions
monkeys as surrogate children. Such alloparenting is common and
(Yohanan & MacLean, 2008). Direct physical contact with social part-
unsurprising since neurologically we are capable of viewing our com-
ners is associated with decreased blood pressure and heart rate, and
panion animals like our own children (Stoeckel, Palley, Gollub, Niemi, &
increased oxytocin, a neurohormone associated with positive feelings
Evins, 2014)
and affiliative behaviors in many species (Carter, Williams, Witt, & Insel,
Primates are used as companion animals in many places (Malone,
1992; Grewen, Girdler, Amico, & Light, 2005; Light, Grewen, & Amico,
Purnama, Wedana, & Fuentes, 2002). Although it is difficult to deter-
2005; Uvnas-Moberg, 1997). Interacting with one’s own dog is even
mine accurately how many primates are kept as pets (Soulsbury, Iossa,
associated with increases in oxytocin, endorphins, and dopamine in
Kennell, & Harris, 2009), the practice even in the US is long-running:
both the dog and its owner (Odendaal & Meintjes, 2003)!
those who read comic books back in the 1970s might remember seeing
Our desire to touch primates and other species reflects our need
advertisements selling squirrel monkeys as affordable companions.
to learn about the natural world. Children appear more interested in
Despite the fact that the US has prohibited the import of primates as
zoo experiences when they can touch the animals, and parents of these
pets (pursuant to the US Code of Federal Regulations, Title 42, section
children often report such direct interactions with the animals as valua-
71.53) since 1975, eleven states still allow private ownership of prima-
ble experiences for their children (Kidd, Kidd, & Zasloff, 1995). As a
tes, including apes, without any permit: Alabama, Kansas, Missouri,
proximal process, our body language of reaching out communicates
Nebraska, Nevada, North Carolina, South Carolina, South Dakota,
both vulnerability and trust. Perhaps we wish to specifically communi-
Virginia, Wisconsin, and Wyoming. The following US allows private
cate to animals that we are friends in a world full of foes. Whatever
ownership of primates with a permit: Idaho, Connecticut (although
the case may be, our drive as a species to interact with animals, and
Great apes are prohibited), Florida (although Great apes and baboons
primates in particular, produces opportunities for disease transmission.
are prohibited), Maine, Michigan, Mississippi, Montana, North Dakota,
And beyond bushmeat, such opportunities are facilitated through our
Oklahoma, Pennsylvania, Rhode Island, and Texas. Despite the
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35
popularity in the U.S., Europe, and many indigenous areas, primates
from humans (Mack & Noble, 1970; Schillaci, Jones-Engel, Engel, &
function as “playthings” in only six of sixty societies surveyed using the
Kyes, 2006), and they do often harbor pathogens that could be trans-
Human Relations Area Files (Gray & Young, 2011). Privately keeping
mitted to humans (Schillaci et al., 2005). This is the same case for many
small monkey species is rather common in Southeast Asia, West Africa,
animals in zoos and in the wild.
and South America (Jones-Engel et al., 2005; Malone et al., 2002).
These pets are usually young animals orphaned as the result of bush-
4 | ANIMALS ON EXHIBIT
meat hunting. In many places where primates are hunted for food, they
are also kept as pets (Mossoun et al., 2015; Wolfe, Prosser, et al.,
Fifty-three species of primates are currently on display within most of
2004; Wolfe, Sreevatsan, et al., 2004).
the two hundred forty-four facilities currently accredited by the Associ-
Unfortunately, many people often underestimate the true conser-
ation of Zoos and Aquariums in the US (Association of Zoos and
vation status of primates, and this seems to be a result due, in part, to
Aquariums, 2016). 183 million people visited these facilities in 2014 (J.
the use of these species in movies, commercials, television shows, and
Wright, personal communication). Other organizations, such as the
online/print media (Ross et al., 2008; Ross, Vreeman, & Lonsdorf,
Pan-African Association of Zoos and Aquaria, the World Association of
2011; Schroepfer, Rosati, Chartrand, & Hare, 2011). Media portrayal of
Zoos and Aquariums, Canada’s Accredited Zoos and Aquariums, Latin
primates make them seem like suitable pets (Soulsbury et al., 2009),
American Zoo and Aquarium Association, European Association of
and in less need of financial contributions for conservation (Tisdell,
Zoos and Aquaria, Japanese Association of Zoos and Aquariums, and
2006). The reality is that the International Union for the Conservation
the Zoo and Aquarium Association Australasia, endorse hundreds of
of Nature’s Red List of Threatened Species currently (November 2016)
facilities worldwide. It is not possible to know precisely how many ani-
lists 259 species of primates as either critically endangered, endan-
mal parks are both publically and privately owned. However, it is con-
gered, or vulnerable. Of these, 59 are critically endangered. In 2015,
servative to conclude that, at a minimum, these places bring together
the US Fish and Wildlife Service ruled (US Code of Federal Regulations,
many exotic species, and this can facilitate pathogen exchange, even in
Title 50, sections 17.11 and 17.40(c)) that all chimpanzees, wild or cap-
the presence of biosecurity measures (Li et al., 2015). Petting zoos can
tive (including animals in zoos and research facilities), are considered
be particularly problematic where children are allowed to feed animals
endangered in accordance with the Endangered Species Act of 1973.
(Bender & Shulman, 2004; Heuvelink et al., 2002). Many zoos and ani-
Ultimately, primates are not suitable as pets. Many of these ani-
mal sanctuaries (and even theme parks, resorts, and restaurants) out-
mals are aggressive toward unfamiliar people (Soulsbury et al., 2009),
side of the US offer interactive experiences like riding on elephants,
and children are more likely to be bitten than adults (Ostrowski, Leslie,
playing with big cat cubs, walking hand-reared cheetahs on leashes,
Parrott, Abelt, & Piercy, 1998). Although the actual number of cases of
and holding and petting primates. These “pay-to-pet” practices argu-
pathogen transmission from pet primates to owners is unknown, a
ably promote mixed messages about animal conservation (i.e., that it is
significant risk of such pathogen transmission likely exists. For example,
acceptable to touch wild animals), as well as provide opportunities for
Klebsiella, hepatitis A, and rabies virus have been transmitted from
pathogen exchange.
some New World species (Favoretto, de Mattos, Morais, Alves Araujo,
Recreational use of natural areas provides people with opportuni-
& de Mattos, 2001; Renquist & Whitney, 1987). Pet macaques in the
ties to interact with wildlife they might not normally encounter, and
US can harbor Macacine herpesvirus 1 (Ostrowski et al., 1998), an
contributes significantly to the economies of biodiversity-rich countries
alphaherpesvirus that can cause fatal meningoencephalitis in humans.
(World Tourism Organization, 2004). International ecotourism is
Owners can also transmit pathogens, some with fatal consequences, to
increasingly seen as a mechanism to facilitate species and habitat con-
their pet primates (Huemer, Larcher, Czedik-Eysenberg, Nowotny, &
servation by increasing public awareness of conservation issues and
Reifinger, 2002; Jones-Engel et al., 2001; Pourrut et al., 2011). In gen-
raising much needed funds (Balmford et al., 2009). These activities
eral, animal trade for the purpose of exotic pet ownership will continue
should attempt to educate visitors while minimizing modification of
to facilitate the emergence of infectious diseases (Chomel, Belotto, &
natural resources (Ceballos-Lascurain, 1996). However, there are often
Meslin, 2007; Karesh, Cook, Bennett, & Newcomb, 2005).
deleterious effects associated with the rapid, and often unmonitored
Other captive primates function as “performance” animals, and
development of ecotourism programs. These can range from local pol-
occupy a niche somewhere between a personal pet and an exhibit ani-
lution and the introduction of invasive species, and the habituation of
mal (i.e., they interact with audiences but are also often cared for in a
animals that make them more vulnerable to poaching, to even acciden-
home; Schillaci et al., 2005). These performing animals can be found
tal injuries and death of tourists taking photographs of themselves
throughout Asia (and parts of Africa and Central and South America to
(Flaherty & Choi, 2016).
lesser degrees) (Hasan et al., 2016), and some are known famously for
Primate-based tourism has a long history (Russon & Wallis, 2014).
Suo-Sarumawashi or “monkey dancing” in Japan (Ohnuki-Tierney,
From the macaques at holy temples in Asia and on the Rock of
1987). Staged interactions for monetary contributions may include
Gibraltar, baboons at the Cape of Good Hope in South Africa, apes in
underwater diving, boxing, dancing, and acrobatics, among others.
protected forests of Africa and Southeast Asia, lemurs on Madagascar,
Photography sessions often accompany these staged performances
and the New World monkeys in Central and South America, to the
(Agoramoorthy & Hsu, 2005). These animals have acquired pathogens
Yaen-koen monkey parks scattered across Japan, traveling to see wild
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MUEHLENBEIN
F I G U R E 1 (A) A very happy tourist with a longtailed macaque (Macaca fasicularis) at the Sangeh Monkey Forest, Bali, Indonesia.
Photograph by M. Muehlenbein. (B) Tourist with longtailed macaque (M. fasicularis) at the Ubud Monkey Forest, Bali, Indonesia. Notice the
animal’s hands in the tourist’s mouth. Photograph by A. Klegarth. (C) Rather mixed feelings from a tourist with longtailed macaques (M.
fasicularis) at the Phra Prang Sam Yot temple in Lopburi Province, Thailand. Photograph by A. Klegarth
or semi-wild (i.e., animals at rehabilitation centers or sanctuaries) prima-
treatment that travel health professionals provide to patients regarding
tes continues to be a popular choice for many tourists. Of the more
risks of nature-based tourism. Responses from 311 participants
than 23,000 visitors to Volcanoes National Park, Rwanda in 2010,
(approximately 12.5% of the membership) reveal that tourists visiting
almost 19,000 went gorilla trekking, contributing over $10 million to
international travel health clinics are not currently being informed
the local economy (Rwanda Development Board, 2016).
adequately about the risks of zoonotic or anthroponotic disease trans-
Despite the benefits, there are some costs associated with this
mission (Muehlenbein & Brink, 2013; M. Muehlenbein & G. Brink, in
nature-based tourism. International tourists exhibit, in general, rather
preparation). Whereas 82% do advise during pretravel consults about
poor knowledge, attitudes, and practices about their health while trav-
limiting contact with wildlife, this is almost exclusively in reference to
eling (Wilder-Smith, Khairullah, Song, Chen, & Torresi, 2004), with low
preventing zoonotic diseases like rabies.
compliance to physician advice (Steffen et al., 2004) and improper use
Those visiting wildlife sanctuaries underestimate the risks of
of chemoprophylaxes (Van Herck et al., 2004). Gastrointestinal and
becoming infected themselves as well as the contribution they may
respiratory tract infections during travel are very common (Rack et al.,
have to the health of other animals (Muehlenbein & Ancrenaz, 2009).
2005), and many people travel without recommended vaccines (Hamer
For example, ecotourists concerned about environmental protection,
& Connor, 2004). While many choose to ignore the risks of travel,
and with recognized travel itineraries to view endangered species, are
some are simply uninformed or misinformed. Health information is not
not adequately protected against many vaccine-preventable diseases
currently available on commercial travel websites (Horvath, Murray, &
(Muehlenbein et al., 2008). They are largely unaware of their true vac-
DuPont, 2003).
cination status, and they underestimate the risks they pose to other
Recently, an online survey of the membership of the International
species. Furthermore, these same travelers to wildlife sanctuaries are
Society of Travel Medicine aimed to assess the types of advice and
oftentimes ill, showing specific signs and symptoms of infection
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MUEHLENBEIN
37
(particularly those associated with respiratory diseases that can easily
contact with the animals, often as the result of local photographers
be transmitted) (Muehlenbein et al., 2010).
encouraging them to do so (Fuentes et al., 2008). And many of these
While visiting these international locations, tourists can be
animals are known to carry Macacine herpesvirus 1, simian virus 40,
exposed to potential zoonoses through animal bites. Biting is very com-
and simian foamy virus (Engel et al., 2002, 2006; Jones-Engel et al.,
mon in certain places, as in Bali, Indonesia where tourists frequently
2006). The actual number of past pathogen transmission events from
interact with longtailed macaques (Macaca fasicularis) (Fuentes &
wild primates to tourists is presently unknown.
Gamerl, 2005). Whereas Gautret et al. (2007) report only 320 cases of
monkey-associated injuries (bites and scratches) between 1998 and
2005 to the GeoSentinel global surveillance network, a more recent
and detailed analysis reveals 1051 cases of monkey bites of travelers
5 | CASE STUDY ON PRIMATE-BASED
TOURISM
reported between 1995 and 2016 (April) (M. Muehlenbein & M. Mendelson, in preparation). Many of these exposures happen at holy tem-
To understand travelers’ willingness to have contact with primates
ples and shrines where monkeys are often tolerated as part of various
(wild, semiwild, and captive) and associated disease risks, travel health
faiths (Figure 1). There are many “monkey temples” found throughout
knowledge, attitudes, and practices (including health status and per-
Thailand, Indonesia, India, Nepal, China, and Taiwan. These areas are
ceived risks), in addition to environmental values, opinions about eco-
popular destinations for international tourists where hand feeding free-
tourism and primate conservation, and opinions about potential
ranging animals (usually macaques and langurs) by tourists is a common
preventative measures of pathogen transmission, Muehlenbein and
occurrence. Despite advertisements to not feed the animals, as well as
team members have completed detailed surveys of adult tourists at
possible fines, visitors in Bali and other places frequently have physical
four locations (Figure 2). First, 656 visitors were surveyed in May 2009
(A) Spectacled langurs (dusky leaf monkey, Trachypithecus obscurus spp.) with visitors at the Monkeyland Primate Sanctuary,
outside Plettenberg Bay, South Africa. Photograph by Isabel Bradley. (B) Tourist with vervet monkey (African green monkey, Chlorocebus
aethiops sabaeus) and its handler in Cockleshell Bay, Saint Kitts, West Indies. Photograph by C. Gallagher. (C) One small part of a very large
troop of Japanese macaques (snow monkeys, Macaca fuscata) at the Takasakiyama Monkey Park, outside Beppu City, Japan. Photograph by
M. Muehlenbein. (D) Tourists observing an orangutan (Pongo pygmaeus morio) Sepilok Orangutan Rehabilitation Centre, outside Sandakan,
Sabah, Malaysia. Note the animal on top of the regulation sign. Photograph by M. Muehlenbein
FIGURE 2
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MUEHLENBEIN
at the Sepilok Orangutan Rehabilitation Centre, located 22 km outside
African green monkeys (vervets; Chlorocebus aethiops sabaeus). Touch-
of the city of Sandakan in the Malaysian state of Sabah, Northern
ing and feeding these animals are encouraged by locals that solicit tou-
Borneo. This facility functions as a center for the rehabilitation of
rists for money.
orphaned, injured, and confiscated orangutans (Pongo pygmaeus morio)
Research protocols were approved by the Institutional Review
and other endangered species. To facilitate public education and gener-
Boards at University of Wisconsin-Milwaukee, Indiana University-
ate operational funds, the public is allowed to view two feedings daily
Bloomington, the University of Texas at San Antonio, and Ross Univer-
of the orangutans and macaques (longtailed and pigtailed; Macaca fasi-
sity School of Veterinary Medicine. Permissions to conduct research at
cularis and Macaca nemestrina). Touching and feeding of animals by the
each location were granted by the Sabah Wildlife Department, the
public are not permitted, but both do happen on occasion. Second, 615
Sepilok Orangutan Rehabilitation Centre, Takasakiyama Monkey Park,
visitors were surveyed in May 2012 at the Takasakiyama Monkey Park
Ross University, and the South African Animal Sanctuary Alliance. Initial
on Mt. Takasaki, located outside Beppu City in the Oita Prefecture of
results presented here (Table 1) are to illustrate differences among
Kyushu island, southern Japan. Here visitors may view daily feedings of
respondent groups. It should be noted that the majority of tourists in
the approximately one thousand free-roaming Japanese macaques
Saint Kitts were from the US or Europe (and were almost all cruise ship
(snow monkey; Macaca fuscata). Touching and feeding of animals here
passengers), most in Malaysia and South Africa were European, and
are not permitted, but both do happen on occasion. Third, 1175 visi-
nearly all in Japan were Japanese (within-country visitors).
tors were surveyed in November 2013, March 2014, and May 2015 at
While there is significant variation among respondents at different
the Monkeyland Primate Sanctuary, a private facility operated by the
locations, detailed analyses regarding the impacts of education, envi-
South African Animal Sanctuary Alliance, just outside of Plettenberg
ronmental attitudes, and other factors on perceived risk are forthcom-
Bay, South Africa. This twelve-hectare forest is home to eleven species
ing. In brief, while a majority of respondents agree that we can give/
of free-roaming primates. The facility operates guided tours and does
get diseases to/from wild primates, a surprising percentage would still
not permit touching or feeding, with these rules enforced strictly.
touch or feed these animals if given the opportunity. Almost half of the
Fourth, 1399 visitors were surveyed in July 2015 and March 2016 on
respondents in Saint Kitts reported touching a primate, with most of
the beaches of Cockleshell Bay and South Friars on the Southeast
these encounters happening on the island itself during the present visit.
peninsula of the island of Saint Kitts, Federation of Saint Kitts and
Close to one hundred people have been scratched or bitten by a wild
Nevis, West Indies. This island is home to approximately 50,000
primate (not occupationally), and this number does not include the
T A B LE 1
Case study results from 3845 tourists
(a) Attitudes on disease transmission
Malaysia
Japan
South Africa
Saint Kitts
% that think people can GET diseases
from wild primates
% that think people can GIVE diseases
to wild primates
92.4
54.0
86.2
87.5
85.8
53.2
84.5
77.7
(b) Attitudes on touching and owning primates
Malaysia
Japan
South Africa
Saint Kitts
% that would touch or feed a wild
primate in given the chance
% that would own a primate as a pet
21.8
65.7
54.8
56.1
NAa
23.8
10.4
17.7
(c) Experience with touching or bites/scratches
Malaysia
Japan
South Africa
Saint Kitts
% that have touched a primate (wild
or pet animal)
% that have been bitten or scratched
by a primate (not occupationally)
NAa
17.7
20.0
47.6
NAa
2.5
2.3
3.8
% that have visited another destination
to specifically view primates
% that were made aware of health
regulations at the destination
47.7
NAa
31.1
10.8
10.7
NAa
29.4
17
(d) Experience at other locations
Malaysia
Japan
South Africa
Saint Kitts
a
NA: data not available because question was not asked on that version of the survey.
|
MUEHLENBEIN
39
cohort of visitors to Malaysia. Perceived risk of disease transmission
of course context-dependent, just as are peoples’ attitudes toward the
appears to be lower in the Japanese cohort, and a higher percentage of
environment and other biota (see the value-based theory for environ-
Japanese respondents report willingness to own a primate as a pet.
ment concern: Stern & Dietz, 1994). In general, those expressing a kin-
There is significant variation in motivation to travel to primate-tourism
ship for or community with nature (the Connectedness to Nature
destinations: many respondents in Malaysia would self-classify as “eco-
Scale: Mayer & Frantz, 2004) should be less likely to harm it, and those
tourists” traveling to specifically view wildlife, whereas almost all
who truly value their place in the biosphere (Schultz & Zelezny, 1999)
respondents in Saint Kitts were cruise ship passengers with much less
should also respect the physical space of other animals. These attitudes
interest in wildlife.
must be cultivated for nature-based tourism to continue to exist. Risk
An additional interesting result follows from an additional survey
communication must be customized and contextualized to different
collected in 2015 in Monkeyland, South Africa. 258 visitors completed
parties of interest if we are to minimize or prevent primate-based
an entrance survey into the facility, were then provided with a standar-
zoonoses and anthroponoses by understanding how and why different
dized, short conservation message (prior to their guided tour) about
people are willing to engage in different emotional and physical interac-
why contact with wild primates can compromise their health and
tions with these animals.
safety, and then asked to complete an exit survey that asked questions
identical to the entrance version. After their tour, respondents reported
being more likely to believe that humans can give diseases to wild primates (generalized linear model; z 5 3.79, p 5 0.00) and were less
likely to report wanting to touch or feed a wild primate (z 5 5.745,
p 5 0.00) or own one as a pet (z 5 2.34, p 5 0.02). Remaining analyses
for this and the other three locations are pending (Muehlenbein et al.,
in preparation).
ACKNOWLEDGMENTS
Access to fieldsites was provided or facilitated by the following:
Sylvia Alsisto, Laurentius Ambu, Marc Ancrenaz, Patrick Andau, Tony
Blignaut, Cecilia Boklin, Lee Dekker, Kerry Dore, Christa Gallagher,
Hideo Hasegawa, Michael Huffman, Sail Jamaludin, Vijver Jonk,
Monkeyland Primate Sanctuary, Lara Mostert, Sen Nathan, Sean
Prall, Raeggae Beach Bar, Ross University School of Veterinary Medicine, Sabah Wildlife Department, Rosman Sakong, Sepilok Orangu-
6 | SUSTAINABLE RELATIONSHIPS
tan Rehabilitation Centre, Shipwreck Bar, Takasakiyama Monkey
Park, Dominik Winkel, and Tim Wright. The following provided assis-
We abuse land because we regard it as a commodity belonging to us.
When we see land as a community to which we belong, we may begin
to use it with love and respect (Leopold, 1949, p. viii)
Researchers have already characterized the risks of human–wildlife
interactions and have provided detailed recommendations on how to
minimize these risks, primarily through physical and behavioral barriers
between ourselves and other species (Gilardi et al., 2015; Homsy,
1999; Macfie & Williamson, 2010; Muehlenbein & Wallis, 2014).
Anthropologists are well suited to investigate cultural variation in motivations for engaging in contact with other species, primates in particular. Risks of pathogen exchange will vary by the contexts of these
interactions, and we must continue to work to understand variation in
risk perception associated with these different activities. Risk will
remain from use of wild animal products until alternative protein sources are identified and accepted. Private ownership of primates and
direct physical touch of wild primates must be discouraged. Unfortunately, humans often choose to participate in self-destructive behaviors
tance with survey collection: Jessieca Audrine, Kelly Baute, Ana
Bouwkamp, Jessica Bryant, Katie Byrd, Kimberly Cook, Hidemi
DeHays, Kerry Dore, Colleen Friedly, Christa Gallagher, Indiana One
Health South Africa class members 2015, Clayrina Julianus, Andrea
Lemke, Leigh Ann Martinez, Emma Morone, Ross University School
of Veterinary Medicine volunteers, and Eric Shattuck. The following
provided assistance with data management: George Armstrong,
Kelsey Black, Hidemi DeHays, Krystiana Krupa, and Leigh Ann
Martinez. I wish to thank Isabel Bradley, Christa Gallagher, and Amy
Klegarth for photographs, Elisha Gray, Martha Lyke, Samantha
Mendoza, and Eric Shattuck for assistance with manuscript production, and Garth Brink, Marc Mendelson, and Robert Steffen for assistance in working with the International Society for Travel Medicine.
Funding for fieldwork was provided by University of WisconsinMilwaukee, Indiana University-Bloomington, and University of Texas
at San Antonio.
if they believe they are pursuing a positive goal (Baumeister & Scher,
1988). This will be particularly the case if they believe the benefits to
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saw one while on vacation? Which post will get the most “likes?”
Ignorance over the risks of wildlife contact cannot fully explain
peoples’ continued desires to interact with primates. These desires to
emotionally and physically engage with other species will continue to
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How to Cite this Article: Muehlenbein MP. Primates on display:
Potential disease consequences beyond bushmeat. Am. J. Phys.
Anthropol. 2017;162:32–43. doi:10.1002/ajpa.23145.