The Welfare and Suitability of Primates Kept as Pets ...€¦ · Fraserincorporate welfare of the individual, of others,andof the environment.This article (a) examines the numbers,

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The Welfare and Suitability of Primates Kept as PetsCarl D. Soulsbury a , Graziella Iossa a , Sarah Kennell b & Stephen Harris aa School of Biological Sciences, University of Bristol , United Kingdomb Royal Society for the Prevention of Cruelty to Animals , West Sussex, United KingdomPublished online: 23 Dec 2008.

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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 12:1–20, 2009

Copyright © Taylor & Francis Group, LLC

ISSN: 1088-8705 print/1532-7604 online

DOI: 10.1080/10888700802536483

ARTICLES

The Welfare and Suitability of PrimatesKept as Pets

Carl D. Soulsbury,1 Graziella Iossa,1 Sarah Kennell,2

and Stephen Harris1

1School of Biological Sciences, University of Bristol, United Kingdom2Royal Society for the Prevention of Cruelty to Animals,

West Sussex, United Kingdom

Amid growing concern about keeping exotic species as companion animals, non-

human primates have been highlighted as inappropriate for private ownership.

However, there has been no comprehensive review of the suitability of primates

as pets, using a framework such as Schuppli and Fraser’s (2000). Schuppli and

Fraser incorporate welfare of the individual, of others, and of the environment. This

article (a) examines the numbers, origins, ages, and ownership trends of primates

kept as pets in the United Kingdom and (b) identifies a number of welfare, health,

and environmental concerns. Overall, strong evidence supports the argument that

primates are not suitable pets; it is unlikely that the welfare of pet primates can

be adequately addressed in normal households. Finally, using unpublished data

on complaints and inquiries received by the Royal Society for the Prevention of

Cruelty to Animals, the study assesses the degree of public concern about the

welfare of primates kept as pets in England and Wales. The article identifies a

wide range of concerns about keeping pet primates and concludes that this practice

should end.

In many countries, there has been growing concern about the increase of ex-

otic species kept as companion animals (American Veterinary Medical Asso-

Correspondence should be sent to Carl D. Soulsbury, School of Biological Sciences, University

of Bristol, Woodland Road, Bristol BS8 1UG, UK. Email: [email protected]

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2 SOULSBURY, IOSSA, KENNELL, HARRIS

ciation, 2000; Animal and Plant Health Inspection Service, 2000; Canadian

Veterinary Medical Association, 2003; Engebretson, 2006; Geffray & Paris,

2001). This concern stems from several reasons. Wild, nondomesticated species

are ill equipped to live in close contact with humans, and many caregivers

(owners) lack the necessary knowledge about the ecology and behavior—and

hence requirements—of the species they keep, thereby causing poor welfare

for many exotic pets (Duarte-Quiroga & Estrada, 2003; Engebretson, 2006;

Jacobson, 1993). Some exotic species such as large carnivores (Diesch, 1982;

Nyhus, Tilson, & Tomlinson, 2003) or venomous snakes, fishes, and spiders (de

Haro & Pommier, 2003; Diesch, 1982) may pose a physical threat to human

health, whereas many commonly kept exotic pets, such as reptiles, can pose a

significant disease risk if keepers do not follow simple health precautions (Ward,

2000; Woodward, Khakhria, & Johnson, 1997).

A further concern is that some exotic pets are sourced from the wild, thereby

contributing to threats to the survival of wild populations (Cuarón, Martínez-

Morales, McFadden, Valenzuela, & Gompper, 2004; Duarte-Quiroga & Estrada,

2003; Eudey, 1994; O’Brien et al., 2003; Perälä, 2005; T. F. Wright et al., 2001).

Some unwanted exotic pets have been released or escaped into the wild, allowing

the establishment of species outside their native range, such as Burmese pythons

(Python molurus), Nile monitors (Varanus niloticus), and Gambian pouched rats

(Cricetomys gambianus) in North America (Enge, Krysko, Hankins, Campbell,

& King, 2004; Perry et al., 2006; Reed, 2005). Concern has now been raised

about their potential as invasive species and the likely disruption to the native

fauna and flora (Enge et al., 2004; Perry et al., 2006). Drawing on these concerns,

Schuppli and Fraser (2000) developed a systematic analysis to evaluate the

suitability of different species as companion animals based on three main criteria:

welfare of the animal, welfare of others (including humans and other nonhuman

animals), and welfare of the environment (including threats to wild populations

through trade and introduced species).

The debate regarding the keeping of nonhuman primates (primates hereafter)

as pets has been ongoing for a number of years; several studies have highlighted

specific aspects of primate husbandry, welfare, and the associated risks to human

health as being important reasons not to keep primates as pets (Keymer, 1972;

Renquist & Whitney, 1987). Veterinarians commonly oppose keeping pet pri-

mates and try to dissuade potential owners (Johnson-Delaney, 1991; Rosenthal,

2000). Recently, there has been renewed debate about keeping pet primates,

including a proposal either to regulate or ban the keeping of primates as pets

in the United Kingdom (Anonymous, 2005a) and the proposed prohibition of

interstate movements of pet primates in the United States (Anonymous, 2005b).

Despite this debate, there is no comprehensive assessment of the suitability of

primates as companion animals within a framework such as that advocated by

Schuppli and Fraser (2000). Hence, this article aims to (a) examine the numbers,

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PRIMATES KEPT AS PETS 3

origin, ages, and social conditions of primates offered for sale within the United

Kingdom and, where possible, globally; (b) review the literature about primates

kept as pets; (c) use the three criteria suggested by Schuppli and Fraser to

assess whether primates make suitable pets; and (d) assess the degree of public

concern about the welfare of primates kept as pets in captivity, using previously

unpublished data on complaints and inquiries received by the Royal Society for

the Prevention of Cruelty to Animals (RSPCA).

SOURCES OF PRIMATES IN THE PET TRADE

Primates kept as pets are derived from three sources primarily, wild individuals

and captive breeding and also from surplus zoo stock. The Convention on

International Trade in Endangered Species of Wild Fauna and Flora (CITES)

lists 49 species of primates in Appendix I, which effectively bans all interna-

tional trade; all other species are in Appendix II, which requires trade to be

regulated (CITES, 2006). In the United Kingdom, an estimated 57% of about

24,000 primates used for research and testing during 1994–2000 were imported

(Prescott & Jennings, 2004). Between 2000 and 2004, about 8,400 primates were

imported into the United Kingdom. Of those imported, 99.3% were destined

for biomedical research or commercial or captive breeding facilities—with just

0.69% for zoo-based captive-breeding and conservation programs. Only one

primate was imported for personal reasons (Parliamentary Questions, 2004).

Consequently, legal importation is not an important source of pet primates in

the United Kingdom.

In the United States, 20% of 383,800 primates used in research and testing

during 1995–2001 were imported (Prescott & Jennings, 2004), but importation

for private use has been illegal since 1975 (Anonymous, 1975). However, accord-

ing to CITES, 828 primates were imported to the United States for “personal

use” between 1975 and 2006, of which 78% were macaques (Macaca spp.;

CITES, 2006). Furthermore, this has done little to reduce the sale of primates

as pets, as captive-bred offspring of animals purportedly imported before 1975

continue to be sold (Ostrowski, Leslie, Parrott, Abelt & Piercy, 1998). Better

regulatory systems in some countries make the importation of primates for the

pet trade harder or unlikely, but illegal smuggling does occur (Hansard, 2005).

Local species are typically kept as pets in countries with native primate

populations. For example, 82% of pet primates in Mexico City belonged to

three native species sourced from the wild (Duarte-Quiroga & Estrada, 2003).

Most species kept as pets in Indonesia were also native to the region (J. Wright,

2005). Many of the primates traded locally were a by-product of the bush-meat

trade (Cowlishaw & Dunbar, 2000; Teleki, 1989), but deliberate targeting of

youngsters or valuable or rare species can occur (Mittermeier, 1987; Nijman,

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2005; J. Wright, 2005). Between 1997 and 2001, Shepherd, Sukumaran, and

Wich (2004) recorded 1,175 primates for sale in the Medan markets of Sumatra;

many were infants with a low probability of survival (Geissmann, Nijman, &

Dallmann, 2006).

Modern zoos are increasingly successful in maintaining and breeding pri-

mates, leading to the production of “surplus” animals (Lindburg, 1991). There

are a number of options open to zoo managers on how to deal with surplus

animals, one of which is to make surplus stock available for trade through

animal dealers (Glatston, 1998; Lewandowski, 2003; Travers & Turner, 2005).

Although zoos often go to considerable efforts to limit second-party transactions,

to prevent unqualified persons from obtaining animals (Lewandowski, 2003),

some animals enter private ownership via this route (Green, 1999). Although

the extent of this problem is unclear, it is likely to be limited.

Because captive breeding by private breeders and dealers is believed to be

the main source of primates in the United Kingdom (Greenwood, Cusdin, &

Radford, 2001) and in other countries without native primates, we examined the

number, species, and age of primates offered for sale on 4 days in 2006 (July 11,

August 15, October 19, and December 14) in classified ads on two UK-based

Web sites. There were three principal taxa: capuchin monkeys, marmosets, and

tamarins (Figures 1a, 1b). Most of the capuchins were infants, usually at the age

of weaning, whereas the marmosets and tamarins were of mixed ages. Given

their age when offered for sale, it seems likely that most primates are being

bred in captivity for the UK pet trade. A recent spate of thefts of primates from

British zoos may be one source of unusual species, or the thefts may augment

captive breeding groups (Hevesi, 2005).

Numbers of Primates Kept as Pets

There are no accurate figures on the number of primates kept as pets be-

cause most countries do not have a recognized body recording the number

or species of privately owned primates. In Great Britain, the private possession

of primates is currently governed by the Dangerous Wild Animals Act 1976

(DWAA), which originally exempted certain primates (Callithrix spp., Cebuella

pygmaea, Hapalemur spp.) from licensing (Department for Environment Food

and Rural Affairs, 2005). However, in October 2007, Avahi laniger, Aotus spp.,

Callicebus spp., Samiri spp., and Saguinus spp. were also exempted (Depart-

ment for Environment Food and Rural Affairs, 2007). As a consequence, the

number of primates held under license does not reflect the actual number of

captive primates. Furthermore, hobbyist groups and the pet trade have estimated

noncompliance with DWAA licenses to be 85–95% (Greenwood et al., 2001).

Because the number of primates held legally under DWAA licenses in England

and Wales ranges between 519 and 655 (Greenwood et al., 2001; Travers &

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FIGURE 1a The number of pet sales of adult and infant primates (see Figure 1b note).

FIGURE 1b Groups or individual primates. Note: Figure 1a and Figure 1b include only

those for sale in classified advertisements in searches carried out on 4 days in 2006: July 11,

August 15, October 19, and December 14.

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Turner, 2005), if noncompliance with DWAA licensing is as high as suggested

earlier, the true number is likely to be an order of magnitude higher. With this

exempting of extra species in October 2007, the exact number of primates in

private ownership will be even harder to estimate. Based on the breakdown of

species held under license in 2005, the number of registered primates would

drop from 519 to 337.

Similar problems occur in the United States. Depending on municipality,

state, and/or species involved, owners may be required to have certain licenses;

however, many owners avoid this regulatory system (Animal Protection Institute,

2005; Johnson-Delaney, 1991). The number of primates kept as pets in the

United States is as high as 15,000 (Born Free USA, 2005). A considerable

number of primates were believed to have been kept as pets in The Netherlands

prior to this being made illegal in 1977, after which the number dwindled (van

der Helm & Spruit, 1988). Japan imported 16,000 primates for the pet trade

every year pre-CITES (Matsubayashi, Gotoh, & Suzuki, 1986). Post-CITES,

this number dropped: between 1981 and 1983, about 7% (569 of 8,553) of

primate importation into Japan was for the pet trade (Matsubayashi et al., 1986).

Within the European Union, imports of live primates represent by far the largest

number amongst CITES-listed mammals (93%), but it is thought that the pet

trade represents only a small market for primates and that the vast majority are

used in biomedical research (Swanson & Luxmoore, 1997).

In countries with wild primate populations, ownership of primates is widespread

but difficult to quantify (Fuentes, 2006). However, the scale of the problem is

indicated by the number of individuals in rescue centers who were former pets

or were offered for sale in markets. In Africa, 75% of 561 rescued bonobos

(Pan paniscus), chimpanzees (Pan troglodytes), and gorillas (Gorilla gorilla)

were either being offered for sale or were previous pets (Farmer, 2002). Despite

being illegal in South Africa, the keeping of pet vervet monkeys (Chlorocebus

aethiops) is common, with sanctuaries holding upward of 3,000 confiscated or

donated individuals (Grobler et al., 2006). In 3 years, 14.5% (40/276) of all

seized or donated wildlife taken to one Mexican zoo were primates, while in the

same period 97 howler monkeys (Alouatta spp.) were received by five Mexican

zoos (Cuarón, 2005). In Costa Rica, 3.2% of 1,021 households reported keeping

or having kept a primate (Drews, 2001). Of the 142 households that reported

keeping a wild mammal species, the most common (31.6%) were primates

(Drews, 2001). There is a similar high level of primate ownership in Indonesia;

Shepherd et al. (2004) recorded 1,175 primates for sale between 1997 and 2001

in the Medan markets of Sumatra, and 30% of respondents in Sulawesi owned

or had previously owned a primate (J. Wright, 2005). Despite being illegal in

India, many primates are offered for sale at markets as pets (Ahmed, 2001).

Culturally, ownership of pet primates is most widespread in south and southeast

Asia, southern Africa, and Central and South America (Fuentes, 2006). Although

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clearly considerable, the total number of primates kept as pets worldwide is

impossible to quantify.

Trends in Numbers of Pet Primates

Although it is difficult to quantify the number of primates kept as pets, estimating

trends in primate ownership is even harder. In The Netherlands, where primate

ownership was common in the 1970s, a ban led to a significant decline in the

numbers of pet primates (van der Helm & Spruit, 1988). In contrast, in the

United Kingdom, the number of primates held under licenses increased until

2001 and has remained stable since then (Greenwood et al., 2001; Travers &

Turner, 2005). Furthermore, the species kept have altered; the number of lemurs

(Lemur spp.) in particular held in private ownership has increased from 10 in

1988 to 120 in 2004 (Baker, 1990; Travers & Turner, 2005).

Primate ownership has also increased substantially in the range states in recent

years (Eudey, 1994; J. Wright, 2005). Thus, globally it is unclear whether primate

ownership is increasing or decreasing. Although the enforcement of regulative

legislation in developed countries may decrease the number of primates kept as

pets, primate ownership continues in the range states despite legislation (Ahmed,

2001; Grobler et al., 2006).

WELFARE OF THE ANIMAL

To assess the welfare of exotic pets, Schuppli and Fraser (2000) considered the

range of factors described by the Farm Animal Welfare Council (1992). These

include the following:

1. Freedom from hunger, thirst, and malnutrition;

2. Freedom from disease and injury;

3. Freedom from physical forms of thermal discomfort;

4. Freedom from fear, distress, and negative psychological states; and

5. Freedom to carry out normal behaviors.

An important criterion for consideration is that these welfare factors should be

covered for the individual’s entire life span, which may be problematic in long-

lived species such as primates. Schuppli and Fraser also incorporate other factors

in a welfare assessment, including whether there is adequate knowledge of the

species and the impact of keeper knowledge/expertise and whether the keeper

loses interest in, or commitment to, the animal. Although these are important

within the context of individual welfare, such things are difficult to quantify;

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thus, although using the framework set out by Schuppli and Fraser, we focus on

more tangible issues to assess whether primates make suitable pets.

Diet

The correct diet is important to ensure primate welfare. For example, New-

world monkeys have high vitamin D3 requirements, as their frugivorous diet

contains more phosphorus than calcium (Krook & Barrell, 1962). Most captive

primates are housed indoors, which means they have insufficient access to

sunlight (Hatt & Sainsbury, 1998) and, in some cases, are clothed by their

owners, preventing sunlight from reaching their skin (Kim, Abee, & Wolf, 1978);

consequently, their vitamin D3 requirements must be met through supplements.

Without supplements, skeletal diseases such as rickets can occur (Liu, 1996;

Resnick, 1971).

Nutrition-related bone diseases are common; over a 4.5-year period from

early 1966, 20.3% of 64 necropsied pet primates had some form of bone disease

(Keymer, 1972). Bone disease in primates kept as pets is a recurrent issue (Hatt

& Sainsbury, 1998; Kim et al, 1978; Resnick, 1971). Other vitamin or mineral

deficiencies include zinc or vitamin C (Chadwick, May, & Lorenz, 1979), and

18.8% of 64 necropsied pet primates had some other general nutritional disorder

(Keymer, 1972).

Although there are now many commercially available primate foods, their

nutritional content does not account for species-specific requirements; thus,

keeping some species in captivity still remains problematic (Crissey & Pribyl,

1997). Moreover, commercial foods are not always provided by owners, and

the provision of poor and inappropriate diets for pet primates appears to be a

common problem (Hatt & Sainsbury, 1998; Hevesi, 2005). Primates kept as pets

may also be given inappropriate items to consume, including coffee, tobacco,

and marijuana (Duarte-Quiroga & Estrada, 2003) or, as in one study, left to

starve; 7 of 36 (19%) pet primates with known fates starved to death (J. Wright,

2005).

Primate health is intrinsically linked to diet (Barnard, Knapka, & Renquist,

1988). In addition to nutritional disorders (Hatt & Sainsbury, 1998; Keymer,

1972; Resnick, 1971), inappropriate or inadequate diet can increase susceptibility

to diseases (Hubbard, 1995; Keymer, 1972), including those of human origin

(Johnson-Delaney, 1991). In Mexico City, of 97 pet primates with ailments,

33% had respiratory, 24% gastrointestinal, 16% skin, and 14% viral disorders;

the other 12% were undefined (Duarte-Quiroga & Estrada, 2003). Though poorly

reported in the scientific literature, cases of fatal transmission of common dis-

eases from humans to pet primates have been noted (Huemer, Larcher, Czedik-

Eysenberg, Nowotny, & Reifinger, 2002; Johnson-Delaney, 1991). A survey of

190 veterinarians in England and Wales found that, in 1 year, 3.5% of treated

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exotic pets were primates (RSPCA, 2004). Given the purportedly low number

of primates kept as pets in the United Kingdom, this small veterinarian sample

suggests a serious problem.

Environmental Housing

Good husbandry for primates is challenging for a number of reasons. In particu-

lar, primates require temperature, humidity, and light levels not found in normal

private households (Hevesi, 2005). Although tolerance of suboptimal tempera-

ture and humidity may vary with species, inappropriate conditions contribute to

health problems. For example, temperature fluctuation is thought to contribute

to the high incidence of respiratory diseases in pet primates in Mexico City,

although lack of access to sunlight may contribute to skin disorders (Duarte-

Quiroga & Estrada, 2003).

Primates have large home ranges, ranging from 0.4 km2 in marmosets to

170 km2 in the largest primates (Mendes Pontes & Oliveira Monteiro da Cruz,

1995; Milton & May, 1976). In captivity, good housing of adequate size and

quality is necessary to ensure good welfare (Prescott & Buchanan-Smith, 2004).

In laboratories, standard cage sizes can be adjusted to body mass (Reinhardt,

Liss, & Stevens, 1996), although species-specific space requirements should

be used to determine optimal cage size (Buchanan-Smith, Prescott, & Cross,

2004; Prescott & Buchanan-Smith, 2004). To the best of our knowledge, there

are no published data on cage and enclosure sizes for pet primates; thus, it

is not possible to comment directly on their impact on primate welfare. It is,

however, necessary to highlight the importance of cage and enclosure sizes in

captive primate welfare and consider whether these provisions can be met in

private households. Keeping primates free roaming in houses or tied outside

can be major causes of injury or mortality. In Mexico City, 30% of primates

suffered injuries or death due to burns, falls, or electrocution (Duarte-Quiroga

& Estrada, 2003). Many primates are kept tied up (Duarte-Quiroga & Estrada,

2003; J. Wright, 2005); in one study, 39% of mortality was due to asphyxiation

caused by the rope tied around the animal’s neck (Duarte-Quiroga & Estrada,

2003).

Social Interactions

Behavioral problems resulting from poor social housing are frequently noted

in pet primates (Johnson-Delaney, 1991). This can stem from two problems:

individual housing and/or separation from maternal or familial care at a young

age. In our search of primates offered for sale in the United Kingdom, 63% of

those on sale were infants (Figure 1a), and 78% were single individuals (Figure

1b). Similarly, 44% and 66% of the two most common species kept in Mexico

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City were infants or juveniles (Duarte-Quiroga & Estrada, 2003). Two studies

in Indonesia found that 58% of pet primates were juveniles (Jones-Engel et al.,

2004) and 44% were infants (J. Wright, 2005).

Individually housed primates show stereotypic behaviors more than group-

housed primates (Spring, Clifford & Tomko, 1997). Furthermore, primates kept

alone also show increased rates of negative or unwanted behaviors including self-

injury, autoerotic stimulation, coprophagia, and excessive locomotion (Honess

& Marin, 2006; Reinhardt & Rossell, 2001). Separation from maternal and

familial conspecifics in primates causes stress-induced physiological changes,

such as elevated cortisol levels and prolonged decreases in leukocyte levels

(Coe, 1993; Norcross & Newman, 1999; Shannon, Champoux & Suomi,

1998). During offspring development, early postnatal parental care is pivotal

in primates; the absence of sensory stimulation and two-way interactions with

the biological mother can lead to short- and long-term psychological and

behavioral problems (Harlow & Harlow, 1962; Kaufmann & Rosenblum, 1967;

Mallapur & Choudhury, 2003; Pryce, Rüedi-Bettschen, Dettling, & Feldon,

2002). Juvenile primates learn through social facilitation and interactions with

similar-age and older conspecifics. This is particularly evident with regard to

food. Juvenile primates show high levels of food neophobia; the presence of

familial conspecifics facilitates the acceptance of novel food items and increases

ingestion rates (Wiens & Zitzmann, 2003; Yamamoto & de Araújo Lopes, 2004).

As a consequence, separation of young primates from maternal and familial

bonds can often also lead to feeding problems.

These “early life” experiences have far-reaching consequences throughout a

primate’s life, as primates separated from their mothers often show reduced or

no reproductive success, increased aggression, decreased survival, and reduced

immunity (King & Mellen, 1994; Lewis, Gluck, Petitto, Hensley, & Ozer, 2000;

Meder, 1989). Hand-reared primates show higher levels of abnormal behaviors

and reduced reproductive success (Marriner & Drickamer, 1994; Roy, 1981).

However, if given appropriate social groupings in later life, some pet primates

can reintegrate into primate groups and show comparatively natural behavior

(Anaya-Huertas & Mondragón-Ceballos, 1998).

The importance of social interaction during infancy is not restricted to contact

with the mother (Harlow & Harlow, 1962). Harlow (1969) reviewed several

studies and highlighted the need for social interactions with similar age con-

specifics for normal development. Without conspecific interactions, individuals

show abnormal social and nonsocial behaviors (Coelho & Bramblett, 1981). As

a consequence, zoos are increasingly recognizing the importance of appropriate

social interaction at a young age, with hand-rearing itself being minimized and

greater emphasis being placed on encouraging maternal competence prepartum;

where primates are hand-reared, they are reintegrated into primate groups earlier

to minimize behavioral problems in later life (Porton & Niebruegge, 2006).

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Normal Behaviors

To express normal behaviors, captive primates require appropriate social con-

ditions and adequate housing, including the provision of environmental enrich-

ment. We have already shown that the social conditions of primates kept as pets

are likely to be poor, and adequate housing, such as space to express normal

behaviors, is likely to be limited. Primates are highly active and require a varied

and stimulatingly environment. In the wild, primates may spend 10–30% of their

time resting and 30–40% feeding/foraging (Fragaszy, 1990; Isbell & Young,

1993; Passamani, 1999). There are no quantitative data about primates kept as

pets; however, in zoos which apply a wide range of enrichments, captive primates

have similar time budgets to those living in the wild (Dalton & Buchanan-

Smith, 2005). It seems reasonable to expect that primates kept as pets, with

less provision for enrichment and social interactions with conspecifics, have

markedly different behavioral time budgets. Pet primates are normally housed

in small, bare environments (Hevesi, 2005) and so are unable to express normal

behavioral budgets. Bare environments lacking enrichment can lead to boredom,

frustration, and the development of abnormal behaviors such as self-directed

biting and stereotypic behaviors (Tarou, Bloomsmith, & Maple, 2005).

WELFARE OF OTHERS

Less consideration is usually given to the interaction between pets and their

owner(s) and/or other animals or the community. However, Schuppli and Fraser

(2000) highlighted that the welfare of others should focus on the (a) physical and

(b) disease risks of the animal to the owner(s), other pets, and/or the community.

Aggression

Aggressive behavior toward humans is particularly common among pet primates

and may lead to serious injuries or death; the risk of injuries is not related to

the size of the primate (Animal Protection Institute, 2005; Captive Wild Animal

Protection Coalition, 2005; Corning, 2005; Diesch, 1982). Children may be more

vulnerable than adults because of inappropriate handling or because, in the wild,

aggression is directed toward the smaller members of the group (Diesch, 1982;

Ostrowski et al., 1998). Aggressive behavior is a pivotal component of social

interactions within wild primate groups, leading to the creation and maintenance

of a social hierarchy (Pereira, 1995; Tokuda & Jensen, 1969). Aggression in-

creases during puberty and is mainly directed toward older conspecifics (Moura,

2003) or, in the case of pet primates, their owners (Duarte-Quiroga & Estrada,

2003). In some species, especially Old-world monkeys, the serious nature of

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bites and aggression may be further exacerbated by the significant risk of

transmitting diseases such as rabies or B-virus (Diesch, 1982; Janda, Ringler,

Hilliard, Hankin, & Hankin, 1990; Ostrowski et al., 1998). Aggression also has

significant welfare implications for the primate; 11% of pet-primate mortality

was due to owners killing pets following an aggressive incident (Duarte-Quiroga

& Estrada, 2003).

Disease Risk

Primates are biologically and physiologically similar to humans, allowing rela-

tively easy disease transmission between primates and humans. Surveys of pet

macaques revealed the presence of antibodies to several human pathogens and

a high proportion (59.1%) had human-derived enteric parasites (Jones-Engel,

Engel, Schillaci, Babo, & Froehlich, 2001; Jones-Engel et al., 2004). Disease

transmission from pet primates to humans is viewed as a major public health con-

cern (Ostrowski et al., 1998; Renquist & Whitney, 1987) as primates can harbor

many dangerous parasitic, bacterial, or viral pathogens (Ialeggio, 1997; Keymer,

1972; Ostrowski et al., 1998; Renquist & Whitney, 1987; Wolfe et al., 1998).

These pathogens can be readily transmitted to owners; for example, an

outbreak of drug-resistant Shigella and Salmonella in humans was sourced

to their primate pets (Fox, 1975; Juan-Sallés, Vergés, & Valls, 1999). Several

serious emerging human pathogens such as Marburg virus, Ebola, monkeypox,

and simian immunodeficiency virus (SIV) originated from, and are harbored

in, primates (Gao et al., 1999; Marx et al., 1991). The close contact afforded

by keeping them as pets and the likelihood of being bitten mean that disease

crossover is highly likely (Wolfe et al., 2004); indeed, pet primates are one

possible route of transmission of human immunodeficiency virus (HIV-1 and

HIV-2) to humans (Gao et al., 1999; Marx et al., 1991).

The risk of zoonotic disease transmission is a key argument against keeping

primates as pets (Juan-Sallés et al., 1999; Renquist & Whitney, 1987). Legally

imported primates have been the source of several human epizootics in Europe

and the United States (Brown, 1997). Whereas certain diseases are screened for

in legally imported primates, thereby reducing the chances of infection (Brown,

1997), many important human diseases are common in wild primate populations.

Because monkeys are also smuggled into countries such as the United Kingdom

(Hansard, 2004), the illegal importation of primates is one route for new diseases

to be introduced into previously unexposed countries (Stephenson, 2003).

Risk to the Environment

In most countries without native primate populations, the majority of pet pri-

mates appear to be sourced through captive breeding. However, in the range

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states, the majority of primates come from the wild. This can involve killing

several individuals for a single infant (Duarte-Quiroga & Estrada, 2003; Eudey,

1994; Teleki, 1989). Local and international transport can incur high rates of

mortality (Duarte-Quiroga & Estrada, 2003; Kavanagh, Eudey, & Mack, 1987).

Consequently, both the local and, to a lesser extent, the international trade in

primates are contributing to the decline in some species (Duarte-Quiroga &

Estrada, 2003; Eudey, 1994).

Pet primates frequently escape. Escapes in Britain (Baker, 1990) are unlikely

to pose a risk to the environment, but the same cannot be true for many other

countries. In Indonesia, of 36 primates with known fates, 33% were released

or escaped (J. Wright, 2005). Escapes of pet macaques (Macaca fascicularis)

in Mauritius led to the establishment of this invasive species on the island

(Sussman & Tattersal, 1986). Similarly, in New Guinea, where the same species

is imported to keep or sell as pets, the risk of escapes forming new populations

is significant (Kemp & Burnett, 2003). Several diseases of anthropogenic origin

have afflicted and threatened the persistence of some primate populations (Wallis,

2000); in addition, the release of pet primates in countries with natural primate

populations, or interactions between wild and pet populations, may facilitate

transmission of human diseases into wild primate populations (Jones-Engel et al.,

2001).

Public Concern

To assess the extent of public concern about the welfare of primates kept as

pets in England and Wales, we analyzed unpublished data from the RSPCA

regarding primate-related complaints. Between 2000 and 2005, a total of 191

primate-related cruelty complaints were received by the RSPCA. The majority

concerned neglect: These complaints involved 446 animals or approximately

70% of the primates then held legally in England and Wales under DWAA

licenses (Greenwood et al., 2001; Travers & Turner, 2005). Because we have

shown that noncompliance with DWAA licensing is likely to be high (up to 85–

95%), these complaints are probably related to a smaller proportion of the total

number of primates kept as pets. Even so, the number of complaints highlights a

significant welfare issue and indicates that the British public is concerned about

the welfare of pet primates.

We then analyzed those 103 complaints in which an RSPCA inspector gave

advice to address welfare concerns. Of these, 64% referred to husbandry issues

such as lack of space or access to food, water, and shelter from adverse weather.

Worryingly, 11.5% of calls regarded some aspect of the primate’s health, in-

cluding mental health (2%). The high proportion of complaints about primate

husbandry and health is consistent with our assumption that these factors are

likely to cause poor welfare for primates kept as pets.

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CONCLUSION

The concept of “suitability” as discussed here takes into account animal and

owner welfare. We have examined the available scientific evidence relating to

the welfare of pet primates and identified three main areas of concern.

First, primate husbandry demands a specialized diet alongside environmental

and social conditions not normally available in common households. As a

consequence, the welfare of many pet primates is likely to be poor.

Second, primates pose a significant physical and disease threat to the owner(s)

and vice versa. Many emerging human pathogens originate from primates; thus,

disease transmission is a major public health concern (Ostrowski et al., 1998;

Renquist & Whitney, 1987). Because of daily owner-pet contact, the risk of

disease transmission is high for primate owners, and many veterinarians advise

against keeping pet primates (Canadian Veterinary Medical Association, 2003;

Johnson-Delaney, 1991; Rosenthal, 2000). On the other hand, pet primates are

equally at risk of disease transmission from their owners (Huemer et al., 2002;

Johnson-Delaney, 1991).

Third, in the United Kingdom, the majority of primates appear to be captive

bred; thus, the trade in pet primates poses little direct threat to wild populations.

However, in developing countries, keeping pet primates is a significant threat

to the persistence of wild populations (Meijaard & Nijman, 2000; Nijman,

2005).

Schuppli and Fraser (2000) used a five-tier system to assess the suitability

of species as companion animals. According to their system, primates fall into

category E: “Species that are unsuitable as companion animals because of undue

risk to one or more of: the animal, the owner, the community or the environment”

(p. 366). In essence, Schuppli and Fraser outlined ethical objections to keeping

companion animals that arise from benefits to the owner to the detriment of

the animal if the animal poses a health or safety risk or if the acquisition or

possession poses a risk to the environment. On the basis of the evidence gathered

in the United Kingdom and worldwide, there appears to be detriment to the

welfare of primates kept as pets, health and safety hazards to the owner(s), and

considerable environmental risk in many countries. With this range of concerns,

it is clear that keeping primates as pets should end.

ACKNOWLEDGMENT

We thank the Royal Society for the Prevention of Cruelty to Animals for funding

this study and Dr. Rob Atkinson for constructive advice.

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