Distress in laboratory animals is usually unnecessary
(Institute for Laboratory Animal Research, 1992, p 85).
The literature makes it clear that the distress resulting from
involuntary permanent confinement in a standard barren cage can
be alleviated by providing the imprisoned primate with:
- compatible companionship,
- foraging opportunities, and
- access to the "safe" vertical dimension.
5.1. Compatible Companionship
Group-housing would be the most species-appropriate refinement
alternative to single-housing. Safe procedures of transferring
single-caged individuals to compatible group-housing arrangements
have been documented for pig-tailed macaques, long-tailed macaques,
and chimpanzees. There is good reason to believe that other species,
such as baboons, stump-tailed macaques, squirrel monkeys, capuchin
monkeys and common marmosets can also be transferred from single-housing
to compatible group-housing arrangements if basic ethological
principles are applied. Attempts with rhesus macaques have so
far been discouraging. This species, as probably all other non-human
primates species, can readily be transferred from single- to social-housing
conditions by carefully pairing adult individuals with same-sex
[to avoid uncontrolled breeding] companions or with naturally
weaned infant companions. Compatible pair-housing has the advantage
over group-housing that individual subjects are readily accessible
and that it does not interfere with common research protocols.
There is a professional consensus that
a compatible conspecific probably provides more appropriate
stimulation to a captive primate than any other potential environmental
enrichment factor (International Primatological Society,
1993, p 11).
National and international regulations and guidelines have
incorporated this assumption in their stipulations and recommendations:
- Any primate housed alone will probably suffer [emphasis
added] from social deprivation, the stress from which may
distort processes, both physiological and behavioural (Canadian
Council on Animal Care, 1984, p 165).
- Social interaction is paramount for well-being. Social
deprivation in all its forms must be avoided. Isolation can only
be justified for short [emphasis added] periods
during the experimental procedure or during essential veterinary
treatment (National Health and Medical Research Council,
1997, p 3 & 5).
- Primates are very social animals. Physical contact, such
as grooming, and non-contact communication through visual, auditory,
and olfactory signals are vital elements of their lives. Providing
animals with a satisfactory social interaction helps to buffer
against the effects of stress, reduce behavioral abnormalities,
increase opportunities for exercise and helps to develop physical
and social competence (Primate Research Institute, 2003,
- Pair or group housing must be considered the
norm [emphasis added]. For experimental animals, where
housing in groups is not possible, keeping them in compatible
pairs is a viable alternative social arrangement. Single caging
should only be allowed where there is an approved protocol justification
on veterinary or welfare [emphasis added] grounds
(International Primatological Society, 2007, p 11).
- Primates should be socially housed as compatible pairs
or groups. They should not be singly housed unless there is exceptional
[emphasis added] scientific or veterinary justification (Medical
Research Council, 2004, p 6-8).
- The remarkable sociality of the primate order in general
is the most relevant characteristic for their humane
[emphasis added] housing (United Stated Department of
Agriculture, 1999, p 17).
- The environmental enhancement plan must [emphasis
added] include specific provisions to address the social needs
of nonhuman primates. (United States Department of Agriculture,
- Single housing should only occur if there is justification
on veterinary or welfare [emphasis added]. Single
housing on experimental grounds should be determined in consultation
with the animal technician and with the competent person charged
with advisory duties in relation to the well-being of the animals
(Council of Europe, 2006, p 14).
Despite the significant importance of housing primates in a
social setting rather than alone, social caging has yet to become
implemented as a standard refinement practice:
- Single or individual caging systems are the basic or staple
housing used for primates. Almost all 'hard' scientific data
have been acquired from singly caged primates (Rosenberg
and Kesel, 1994, p. 459 & 460).
- The common practice of housing rhesus monkeys singly calls
for special attention (National Research Council, 1998, p
Two independent surveys of primate facilities located in the
United States revealed that the percentage of indoor caged macaques
housed socially did not increase over a time period of nine years
(Table 2). Both, in 1994 and in 2003 only about one third of the
animals lived with one or several partners, while two thirds were
living alone (Baker et al. 2007).
2. Percentage of indoor
caged macaques housed in US facilities with one or several companions
in a 1994-survey (Reinhardt, 1994) and in a 2003-survey (Baker
et al., 2007)
Some primatologists have taken the side of the traditional
single-caging practice, probably because any changes to the traditional
housing practices could invalidate the precious historic database
(Dean, 1999) and upgrading the standard caging system would require
extra funds (Crockett, 1993; Crockett and Bowden, 1994).
The following arguments have been brought forth against the
transfer of single-caged primates - especially rhesus macaques
- to social-housing arrangements:
- The rhesus monkey is extremely nervous and energetic and
is difficult to house. Unquestionably [emphasis added],
animals involved in experiments should be housed in individual
cages (Gisler et al., 1960, p 760).
- Any [emphasis added] plan to increase social
interaction also increases the risk of injury and death. Unless
they have grown up in the same social group, primates are not
likely to tolerate each other when placed together as adults.
Besides the risk of trauma, there are other disadvantages to
allowing increased social interaction. Contact between animals
may lead to greater transmission of infectious diseases (Line,
1987, p 858).
- Especially when new pairs are formed and dominance relationships
are being established, there is a strong likelihood that the
veterinarian will be kept quite busy suturing wounds [emphasis
added] (Coe, 1991, p 79).
- When adult rhesus monkeys are first paired there are always
[emphasis added] injuries incurred (Rosenberg and Kesel,
1994, p. 470).
- The possible behavioral advantages of pair housing may
be offset by the increased potential of contagious diseases,
for wounding, and for undernourishment in the less dominant partner
(Novak and Suomi, 1988, p 769).
- Pairing is not uniformly beneficial, however. The animals
usually form dominance relationships, and the subordinate partner
may be subject to behavioral depression or distress (Line
et al., 1989, p 105).
- Social pairing is [emphasis added] associated
with high health risks to monkeys (Morgan et al., 1998, p
- Long-term housing with the same partner may sometimes
lead to boredom, as expressed by a decline in social interaction
and an increase in general passivity (Novak and Suomi, 1988,
The reviewed published data make it quite clear that nonhuman
primates - including rhesus monkeys - can readily be transferred
from single- to pair-housing and some species to group-housing
settings if basic ethological principles are applied to
minimize the risk of injurious aggression related to the establishment
of dominance-subordinance relationships.
Published data also indicate that the health risks tend to
decrease rather than increase when single-caged animals
are transferred to compatible pair-housing arrangements. There
is not one published record demonstrating that subordinate partners
of compatible pairs suffer from undernourishment; this is probably
due to the fact that food sharing is one criteria of partner compatibility.
There is also no published case showing that long-term pair-housing
with the same partner leads to boredom, with the two companions
showing a decline in their motivation to interact with each other.
Being separated from each other during post-operative recovery,
food-intake, metabolic and neurophysiological studies is likely
to distress paired companions. The published literature offers
practical guidance on how partner separation can be avoided during
common research protocols without jeopardizing the safety of the
animals and the scientific integrity of the study.
The transfer to compatible social-housing provides previously
single-caged primates not only with a living environment that
can cure them from the behavioral pathology of self-injurious
biting and help them cope with potentially distressing situations,
but it also enhances their general well-being by allowing them
to be what they truly are: social rather than solitary
animals. Living with one or several conspecifics makes it possible
for the caged primate to actively express his or her biologically
inherent need to engage in social behaviors.
The reviewed literature offers numerous options making it possible
for caged primates to get more involved in food searching, food
retrieving, and food processing activities, thereby allowing them,
at least partially, to satisfy their biological urge to forage.
The most practical, least expensive, yet effective way of feeding
enrichment is the presentation of the daily food ration in such
a way that the animals can work for it.
The importance of foraging opportunities for the well-being
of caged nonhuman primates is underscored and clearly addressed
by some professional guidelines and legal rules, while others
do acknowledge foraging behavior but fail to recommend that it
should be actively encouraged in captive animals.
- The International Primatological Society (1993, p 9-10) recommends
in its Codes of Practice that:
Opportunities should be provided for primates to express most
normal behavior patterns. Opportunities for increased foraging
are ranked as the first, most important ones of particular
benefit. Foraging time can be increased by providing some of
the animal's food in such a way as to make its delivery or discovery
unpredictable. As animals like to work for their food, increasing
processing time, increasing foraging, or providing puzzle feeders
or other feeding devices is encouraged (International Primatological
Society, 2007, p 16).
- The Medical Research Council (2004, p 9) states in its Best
Practice in the Accommodation and Care of Primates used in Scientific
Foraging enhances welfare and minimizes the expression of
abnormal behaviors. Therefore, all primates should be
given the opportunity to forage daily, by scattering food in
litter or substrate on the floor, or in a tray, and by using
devices that encourage foraging activity (e.g., puzzle feeders).
The Medical Research Council will require justification for
the use of scientific procedures that restrict the opportunity
- The Council of Europe (2006, p 48) stipulates in its Appendix
A of the European Convention for the Protection of Vertebrate
Animals Used for Experimental and Other Scientific Purposes (ETS
No. 123) that:
Presentation and content of the diet should be varied to provide
interest and environmental enrichment. Scattered food will encourage
foraging, or where this is difficult, food should be provided
which requires manipulation, such as whole fruits or vegetables,
or puzzle-feeders can be provided.
- The United States Department of Agriculture (1995, §3.81(b))
lists in its Animal Welfare Regulations for nonhuman primates:
varied food items, using foraging or task-oriented feeding
methods as examples of environmental enrichment,
but falls short to stipulate that such methods should be an integral
part of the environmental enhancement plan.
- The National Research Council (1996, 1998) does not offer
clear guidance and fails to recommend the provision of foraging
possibilities for nonhuman primates:
- The National Research Council's Guide for the Care and
Use of Laboratory Animals (1996, p 40) simply notes that:
In some species (such as nonhuman primates) and on some
[emphasis added] occasions, varying nutritionally balanced
diets and providing "treats," including fresh vegetables,
can [emphasis added] be appropriate and improve
- The National Research Council's book, The Psychological
Well-Being of Nonhuman Primates (1998, p 39) briefly mentions
Feeding can [emphasis added] be used
to provide positive behavioral stimulation as a means of enhancing
Access to the Vertical Dimension
There is a professional and regulatory consensus that caged
nonhuman primates need to have access to high structures in order
to feel relatively safe:
- Under natural conditions, many primates spend much of
their lives above ground and escape upward to avoid terrestrial
threats. Therefore, these animals might perceive the presence
of humans above them as particularly threatening (National
Research Council, 1998, p 118).
- The vertical dimension of the cage is of importance and
cages where the monkey is able to perch above [emphasis
added] human eye level are recommended (International
Primatological Society, 1993, p 11).
- Cages should be designed and constructed so that the space
[is] enough to allow for an appropriate rest structure (Primate
Research Institute, 2003, Chapter VI). Perches and three-dimensional
structures should be arranged to make as much use of the available
space as is possible (Primate Research Institute, 2003, Chapter
- The volume and height of the cage are particularly important
for macaques and marmosets, which flee upwards when alarmed.
Their cages should be floor-to-ceiling high whenever possible,
allowing the animals to move up to heights where they feel secure.
Double-tiered cages should not be used since they restrict the
amount of vertical space available to the animals (Medical
Research Council, 2004, p 7). A two-tiered system is not recommended
as these cages are usually too small. The lower tiers do not
allow primates to engage in their vertical flight response, are
often darker, and animals in the lower cages tend to receive
less attention from attending personnel (International Primatological
Society, 2007, p 12).
- The flight reaction of non-human primates from terrestrial
predators is vertical, rather than horizontal; even the least
arboreal species seek refuge in trees or on cliff faces. As a
result, enclosure height should be adequate to allow the animal
to perch at a sufficiently high level for it to feel secure.
The minimum enclosure height for caged marmosets and tamarins
is 1.5 m; the minimum enclosure height for caged squirrel monkeys,
macaques, vervets and baboons is 1.8 m [emphasis added].
It is essential that the animals should be able to utilize
as much of the volume as possible because, being arboreal, they
occupy a three-dimensional space. To make this possible, perches
and climbing structures should be provided (Council of Europe,
2006, p 42,52,54).
Access to the vertical dimension addresses the caged monkey's
biological urge to retreat to and rest in the relatively safe
arboreal dimension of the living quarters. Animal welfare regulations
downplay the importance of elevated resting surfaces, such as
perches, when they merely list these as optional examples of
environmental enrichments (United States Department of Agriculture,
A high perch does not really "enrich" the environment
of a caged primate but it is a necessity for the animal
and, hence, should be a mandatory standard furniture of every
cage in which nonhuman primates are kept. The reviewed literature
attests that high perches can easily be installed both in standard
and squeeze-back cages and that the animals do make consistent
use of them.
Positive Reinforcement Training
It is obvious that a monkey or ape is distressed when he or
she is removed from the familiar home cage, forcefully restrained
and then subjected to a life threatening procedure such as injection
or venipuncture. It is also obvious that a monkey or ape is less
distressed or not distressed at all when he or she has been trained
to cooperate, rather than resist during handling procedures. Professional
guidelines and regulatory stipulations take this circumstance
- Procedures that reduce reliance on forced restraint are
less stressful for animals and staff, safer for both, and generally
more efficient (National Research Council, 1998, p 46).
- Restraint procedures should only be invoked after all
other less stressful procedures have been rejected as alternatives
(Canadian Council on Animal Care, 1993, p 92).
- Physical stress, such as physical or chair restraint,
most definitely affects the behavior and psychology of laboratory
animals. All possible measures to reduce their incidence should
be taken. Animals should be trained to be as cooperative as possible
to the procedures to facilitate the rapid completion of work
and to alleviate stress in both the animals and people in charge
(Primate Research Institute, 2003, Chapter IV).
- Primates of many species can be quickly trained using
positive reinforcement techniques to cooperate with a wide range
of scientific, veterinary and husbandry procedures. Such training
is advocated whenever possible as a less stressful alternative
to traditional methods using physical restraint. Techniques that
reduce or eliminate adverse effects not only benefit animal welfare
but can also enhance the quality of scientific research, since
suffering in animals can result in physiological changes which
are, at least, likely to increase variability in experimental
data and, at worst, may even invalidate the research. Restraint
procedures should be used only when less stressful alternatives
are not feasible (International Primatological Society, 2007,
- The least distressing method of handling is to train the
animal to cooperate in routine procedures. Advantage should be
taken of the animal's ability to learn (Home Office, 1989,
- Primates dislike being handled and are stressed by it;
training animals to cooperate should be encouraged, as this will
reduce the stress otherwise caused by handling. Training the
animals is a most important aspect of husbandry, particularly
in long-term studies. Training can often be employed to encourage
the animals to accept minor interventions, such as blood sampling
(Council of Europe, 2006, p 48).
Despite these common-sense recommendations and the published
fact that primates can readily be trained to cooperate during
common handling procedures, there is resistance to implement positive
reinforcement training as a standard refinement practice in biomedical
research institutions. The reason for this inertia of tradition
is probably related to misconceptions that have been published
in text books and scientific articles:
- All [emphasis added] monkeys are dangerous
(Ackerley and Stones, 1969, p 207).
- Rhesus monkeys in the laboratory have well-earned reputations
for their aggressive response and near-intractable disposition
(Bernstein et al., 1974, p 212).
- Old World primates are [emphasis added] aggressive
and unpredictable (IACUC Certification Coordinator, 2008,
- Nonhuman primates are [emphasis added] difficult
and dangerous to handle (Henrickson, 1976, p 62).
- One of the major drawbacks to the use of nonhuman primates
is that they can be difficult and even dangerous to handle. Restraint
is therefore necessary [emphasis added] and
desirable to protect both the investigator and the animal
(Robbins et al., 1986, p 68).
- Primates can injure personnel severely if adequate restraint
is not used. The risk of herpes virus B infection and other zoonoses
transmitted by bite or scratch is minimized by appropriate restraint
which may be physical or chemical or a combination of the two
(Whitney et al., 1973, p 50).
- Adult male rhesus monkeys are [emphasis added]
aggressive animals and very difficult to handle. Hence experimental
manipulations necessarily involve the use of restraint procedures,
either chemical or physical (Wickings and Nieschlag, 1980,
- Nonhuman primates, no matter how small, can be a danger
to handlers. Restraint is necessary [emphasis added]
to allow sample collection, drug administration or physical
examination (Panneton et al., 2001, p 92).
The reviewed literature suggests that these rather sweeping
statements, albeit made by scientists, are based on beliefs rather
than facts. That they are taken at face value by other scientists
is regrettable as it promotes one of the most important extraneous
variables, namely restraint stress. It is an irony that nonhuman
primates are forcefully restrained in order to protect the handling
personnel, yet despite rigorous observance of all precautions,
bites and scratches are frequent (Valerio et al., 1969, p
45; cf. Zakaria et al., 1996; Sotir et al., 1997) because the
animals are pushed into situations in which they have no other
option but defend themselves. When they have been trained to cooperate,
they work with rather than against the handling
personnel. Under these conditions handling procedures with primates
are safe because the animals no longer have any reason to bite
or scratch in self-defense.
The published reports on successful training protocols for
injection, blood collection, semen collection, saliva collection,
blood pressure measurement, oral drug administration, topical
drug administration and weighing are encouraging. Their systematic
application in the species for which they were originally developed,
and their adaptation to other species will make the handling procedures
with nonhuman primates more "humane" and the research
data collected scientifically more valid.
The traditional housing and handling practices of caged primates
expose the animals to unnecessary distress, which is not
only an ethical concern - distress is a sign of impai red
well-being - but also a scientific concern - distress is an uncontrolled
variable that increases statistical variance.
It is documented in professional and scientific journals that
housing and handling practices of caged nonhuman primates can
be refined, without undue labor and expenses, in such a way that
distress responses are minimized or avoided if basic ethological
principles are applied to:
- address the animals' need to be with and interact with at
least one compatible conspecific;
- structure their living quarters in species-appropriate ways;
- address their biologically strong motivation to forage;
- train them to cooperate during procedures.
With a little bit of good will and earnest concern for animal
welfare and scientific methodology, the systematic implementation
of Refinement for caged nonhuman primates is a practical option.
It must be remembered that the goal of Refinement is to decrease
the incidence or severity of inhumane practices (Russell
and Burch, 1992). The National Research Council (1985, p1) of
the United States:
- claims that the scientific community [has] long
recognized both a scientific and an ethical responsibility for
the humane [emphasis added] care of animals,
- admonishes that all who care for or use animals in research,
testing and education must assume responsibility for their general
welfare [emphasis added].
Is it humane and does it promote animal welfare
when animals, who are known to have strong social needs, are kept
alone in single-cages on a permanent basis?
Is it humane and does it promote animal welfare
when animals, who show a biological vertical flight response,
are permanently kept in cages without a high resting surface?
Is it humane and does it promote animal welfare
when animals, who are highly motivated to engage in foraging behavior,
receive their daily food ration in such a way that no effort is
required to search, retrieve and process the food?
Is it humane and does it promote animal welfare
when intelligent animals, who could readily learn how to cooperate,
are forcefully restrained during common procedures?
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