151
© 2004 Universities Federation for Animal Welfare
The Old School, Brewhouse Hill, Wheathampstead,
Hertfordshire AL4 8AN, UK
Animal Welfare 2004, 13: 151-158
ISSN 0962-7286
Cage sizes for tamarins in the laboratory
MJ Prescott* and HM Buchanan-Smith†
* Research Animals Department, Royal Society for the Prevention of Cruelty to Animals, Wilberforce Way, Southwater, Horsham,
West Sussex RH13 9RS, UK
†
Department of Psychology, University of Stirling, Stirling FK9 4LA, UK
* Contact for correspondence and requests for reprints: [email protected]
Abstract
Provision of adequate space for captive animals is essential for good welfare. It affects not only their behaviour but also determines
whether there is sufficient room for appropriate environmental enrichment. Most importantly, appropriate cage size permits captive
animals to be housed in socially harmonious groups and to fulfil their reproductive potential. For animals used in the laboratory, the
environment can be an additional source of suffering and distress. If they can be better housed and cared for to reduce the overall
impact of experiments upon them, then we are obliged to do so for ethical, legal and scientific reasons. Practically all current guidelines specify minimum cage sizes for laboratory primates based on unit body weight. We believe that no single factor is sufficient to
determine minimum cage sizes for primates, and that instead a suite of characteristics should be used, including morphometric, ecological, social and behavioural characteristics. Here we explore the relevant differences between tamarins (Saguinus labiatus and
S. oedipus) and marmosets (Callithrix jacchus) that have a bearing on setting minimum cage sizes. These include: body size; arboreality and cage use; home range size, mean daily path length and stereotypic behaviour; breeding success in the laboratory; and
species predisposition and aggression. We conclude that it is even more important to provide tamarins with a good quantity of space
in the laboratory than it is marmosets if well-being and breeding success are to be maximised.
Keywords: animal welfare, breeding success, colony management, common marmoset, cotton-top tamarin, red-bellied tamarin
Introduction
Good housing (adequate quantity and quality of space) is
important for all captive animals. For animals used in the
laboratory, the environment can be an additional source of
suffering and distress. If they can be better housed and cared
for to reduce the overall impact of experiments upon them,
then we are obliged to do so for ethical, legal and scientific
reasons. Refining laboratory animal housing and husbandry
to minimise suffering and distress and enhance well-being
is an important and internationally accepted principle.
Two criteria are generally used to assess the well-being of
captive non-human primates (hereafter referred to as primates): the amount and complexity of natural behaviours,
and the incidence and frequency of abnormal behaviour
(Poole 1988). In keeping primates in the laboratory, the goal
should be to provide an environment that maximises the former and minimises the latter. Cage size and complexity are
obvious variables that must be taken into account in achieving this goal. Both variables are important features of the
environment for callitrichids in captive environments (Box
1988, 1995; Chamove & Rohrhuber 1989; Molzen &
French 1989; Schoenfeld 1989; Caine & O’Boyle 1992).
Increasing cage size and/or complexity in the laboratory has
been shown to increase exploratory and play activities and
reduce stereotyped and stress-related behaviour, both in
Universities Federation for Animal Welfare
tamarins (Saguinus) and marmosets (Callithrix) (Box &
Rohrhuber 1993; Kerl & Rothe 1996; Kitchen & Martin
1996; Gaspari et al 2000). Although data on this issue are
inconsistent for macaques in the laboratory (see Reinhardt
& Reinhardt 2001), similar findings have been reported for
significant increases in useable space (eg Draper & Bernstein
1963; Paulk et al 1977; Woodbeck & Reinhardt 1991).
Although fewer tamarins are kept in laboratories than marmosets (generally for specialised areas of research, particularly in the fields of immunology, virology and oncology),
both are typically kept in the same sized cages. This is largely because current UK, European and International guidelines on the housing and husbandry of laboratory animals
specify the same minimum cage sizes for marmosets and
tamarins based on them having body weights under 1 kg
(Council of Europe 1986; European Community 1986;
Royal Society/Universities Federation for Animal Welfare
1987; Home Office 1989; Poole et al 1994; Institute of
Laboratory Animal Resources 1996) (Table 1).
We believe that no single factor, such as body weight, is sufficient to determine minimum cage size for primates in the
laboratory. Instead a suite of characteristics should be used
that include morphometric, ecological, social and behavioural characteristics. (Ideally, one should also take into account
the species, number, age, sex and histories of individuals.)
Science in the Service of Animal Welfare
152 Prescott and Buchanan-Smith
Table 1 Space allowances for marmosets and tamarins specified in various guidelines on the housing and husbandry
of laboratory animals.
Guideline
Category
Minimum cage floor
area (m2)
Minimum cage
height (m)
Council of Europe 1986
<1 kg
0.25 (1–2 animals)
0.6
European Community 1986
<1 kg
0.25 (1–2 animals)
0.6
Royal Society/Universities Federation for
Animal Welfare 1987
0.025–0.65 kg (non-breeding)
0.30–0.65 kg (breeding)
0.25 (1–2 animals)
0.8 (2–6 animals)
1.0 (2–8 animals)
0.8
1.0
1.0
Home Office 1989
Up to 0.7 kg
0.135 (per animal in groups)
0.25 (per animal housed
singly)
0.8
1.0
Poole et al 1994
Callithrix
1.0 (1–2 animals)
1.5
Institute of Laboratory Animal Resources 1996
<1 kg
0.149 (per animal)
0.51
Table 2 Space allowances for marmosets and tamarins in the UK Home Office Code of Practice for the Housing and
Care of Animals in Designated Breeding and Supplying Establishments (Home Office 1995).
Minimum cage floor
area (m2)
Minimum cage
height* (m)
Minimum floor area
per animal (m2)
Breeding pair plus one generation of offspring
0.55
1.5
–
Family group (eight animals maximum)
1.0
1.5
–
Post weaning stock or adults
0.55
1.5
0.135
Family group
1.5
1.5
–
Post weaning stock or adults
1.5
1.5
0.15
Marmosets
Tamarins
* Top of the cage must be a minimum of 1.8 m from the floor.
Guidelines from the International Primatological Society
(IPS) (1993) and Primate Vaccine Evaluation Network
(Poole & Thomas 1995) do not set minimum cage sizes,
although the IPS guidelines do list those set by other bodies,
including the Council of Europe and European Community.
These are directly criticised by the IPS for failing to provide
for the different space requirements of different species.
The only guideline on the housing and husbandry of laboratory primates to specify different (larger) minimum cage
sizes for tamarins than for marmosets is the UK Home
Office Code of Practice for the Housing and Care of
Animals in Designated Breeding and Supplying
Establishments (Home Office 1995) (Table 2). The Code of
Practice states that tamarins are larger animals than marmosets and more excitable, and that in the wild they range
far more widely than marmosets and should be provided
with more space in captivity.
Recently there has been amongst the scientific research
community an increasing awareness of the different needs
of primates at the genera and species level, and of the
importance of meeting these needs in the laboratory environment (eg the ongoing revision of Appendix A to the
© 2004 Universities Federation for Animal Welfare
European Convention for the Protection of Vertebrate
Animals Used for Experimental and Other Scientific
Purposes [Council of Europe 1986]). Regarding tamarins
and marmosets, simply lumping them together as small
New World primates and housing them in exactly the same
way is now considered by many to be unacceptable and to
reflect a poor attitude to research using these animals.
Saguinus and Callithrix are different genera with different
biological requirements and needs, and this ought to be
reflected in their housing and husbandry in the laboratory.
In this paper we explore relevant differences between
tamarins and marmosets that have a bearing on setting minimum cage sizes. These include body size; arboreality and
cage use; home range size, mean daily path length and stereotypic behaviour; breeding success in the laboratory; and
species predisposition and aggression. There is a broad range
of marmoset and tamarin species, with different biological
requirements and needs in captivity (Carroll 1997; BuchananSmith 2001), so a direct comparison between the genera
Saguinus and Callithrix would not be appropriate to the laboratory context. For the purposes of this paper, the very widely bred and used marmoset species, the common marmoset
(Callithrix jacchus), is compared with the most frequently
Cage sizes for tamarins 153
Table 3 Body weights for wild-caught and captive C. jacchus, S. labiatus and S. oedipus.
Species
C. jacchus
S. labiatus
Weight (g)
Average
Range
wild-caught
333 (n = 10)
–
Ferrari 1993
captive-bred
–
Poole & Evans 1982
captive-bred
434 (males)
530 (females)
288
–
Ross 1988
captive-bred
–
360–600
Poole et al 1999
captive-bred
–
350–450
Clarke 1994
captive-bred
–
350–400
Bruhin 1979
captive-bred
–
300–310
Hearn et al 1978
wild-caught
491 (n = 170 males)
–
Yoneda 1981
wild-caught
–
–
F Encarnacion unpublished data in
Snowdon & Soini 1988
Buchanan-Smith 1991
captive-bred
477
515
460
455
–
300–575
Ogden & Wolfe 1979
wild-caught
432 (n = 25 males)
–
Hershkovitz 1977
wild-caught
–
Neyman 1977
wild-caught
410 (n = 21 males)
420 (n = 22 females)
–
404–417
Savage 1990; Savage et al 1993
captive-bred
416.5
–
Ross 1988
captive-bred
562 (n = 90 males)
593 (n = 54 females)
–
McGrew & Webster 1995
captive-bred
490 (males)
480 (females)
–
Kirkwood & Stathatos 1992
captive-bred
–
565–700
Savage 1990; Savage et al 1993
wild-caught
S. oedipus
Reference
(n
(n
(n
(n
=
=
=
=
34 males)
18 females)
6 males)
3 females)
used tamarin species: the red-bellied tamarin (Saguinus labiatus) and the cotton-top tamarin (Saguinus oedipus).
Discussion
Body size
Adult C. jacchus have an average head and body length of
18.7 cm (15.8–20.7 cm) and an average tail length of 28 cm
(24.3–31.2 cm) (Hershkovitz 1977). Adult S. labiatus and
S. oedipus are larger with an average head and body length
of 26.1 cm (23.4–30.0 cm) and 23.2 cm (20.6–24.3 cm) and
an average tail length of 38.7 cm (34.5–41.0 cm) and
37.2 cm (33.3–40.2 cm) respectively (Hershkovitz 1977).
Wild-caught C. jacchus weigh around 330 g, and although
some overweight captive animals fed on a high protein diet
may weigh as much as 600 g (Poole & Evans 1982), most
adults weigh between 300–450 g in captivity. Wild-caught
S. labiatus and S. oedipus weigh between 400–535 g, with
their captive counterparts weighing between 300–700 g
(Table 3). In laboratory cages, larger, heavier primates can
be expected to require more space for locomotion, exploration and exercise. That said, no single factor such as body
weight or body size is a sufficient criterion for determining
minimum cage size. Even species whose weights overlap
may have quite different propensities and needs.
Arboreality and cage use
Whilst both tamarins and marmosets are highly arboreal,
tamarins occupy a higher mean height in the forest (S. labiatus = 17 m [Buchanan-Smith 1991]; C. jacchus = normally below 12 m [Stevenson & Rylands 1988]). S. labiatus
generally spends its time above 10 m, and very rarely
descends to the forest floor (Izawa 1975; Yoneda 1981;
Pook & Pook 1982). In one 5.5-month field study, it was
never seen on the ground (Buchanan-Smith 1991). S. oedipus spends the majority of its time higher than 8 m in the
forest (A Savage personal communication to BuchananSmith 2002). The only time it goes to the ground is if it has
fallen or needs to cross open pasture (Neyman 1980;
A Savage personal communication to Buchanan-Smith
2002). It is incredibly nervous when on the ground and has
been seen to cross ground only twice in 16 years of study by
Savage. In contrast, C. jacchus normally occupies the lower
forest strata, below 12 m, frequently spends time within 1 m
above ground level, and will even go to the ground to pick
up fallen fruits (Stevenson & Rylands 1988).
In captivity, S. labiatus spends 90% of its time in the upper
half of its cage (0.76 × 0.94 × 1.86 m high) when observations are made from a hide, despite adequate furnishing and
food being available in the lower half (Buchanan-Smith
1991). When given a choice of nest box height or foraging
Animal Welfare 2004, 13: 151-158
154 Prescott and Buchanan-Smith
height, it prefers to sleep and feed as far away from the floor
as possible (Caine et al 1992; Prescott & Buchanan-Smith
2002). Similarly, in captivity, S. oedipus also shows considerable reluctance to approach the floor (Snowdon & Savage
1989), especially when bare of substrate (Chamove 1989a),
and spends most of its time above 1 m in cages 2.3 m high
(Snowdon et al 1985). Although in some laboratories
C. jacchus spends more time in the top half of its enclosure
(Kerl & Rothe 1996; Ely et al 1998; Buchanan-Smith et al
2002), it does not show as pronounced a reluctance to
approach the floor as do the tamarin species. It will forage
and even play on the cage floor (Poole et al 1999;
Buchanan-Smith personal observation).
Provision of adequate useable space is essential for good
welfare. The strong predisposition of tamarins to avoid the
lower half of their enclosure, effectively reduces the cage
volume available to them and must be taken into account
when deciding space allowances. If cage height cannot be
increased due to ceiling height, cage cleaning requirements
or ease of capture, the only way to increase useable cage
space is to increase the cage floor area.
Home range size, daily path length and stereotypic
behaviour
Although some marmosets are known to have home ranges
as large as 35.5 ha (eg C. flaviceps), C. jacchus has a small
home range of 0.5–6.5 ha because of its specialisation in
gummivory (Maier et al 1982; Hubrecht 1985; Stevenson &
Rylands 1988; Alonso & Langguth 1989; Scanlon et al
1989). Although home ranges of over 100 ha have been
reported for mixed-species troops of S. fuscicollis and
S. imperator (Terborgh 1983), and S. fuscicollis and S. mystax (Peres 1992), S. labiatus has a home range of
16.75–41 ha (mean = 33.5 ha, n = 4 groups [Yoneda 1981;
Pook & Pook 1982; Buchanan-Smith 1991]) and S. oedipus
has a home range of 7.8–12 ha (Neyman 1977; Savage 1990).
C. jacchus has a daily path length of 100–1000 m/day
(Stevenson & Rylands 1988; Ferrari & Lopes Ferrari 1989).
Whereas S. labiatus has a mean daily path length of
1495 m/day (range = 695–2298 m [Buchanan-Smith 1991])
and S. oedipus has a mean daily path length of 1750 m/day
(Neyman 1977). In fact, in all tamarins species for which
quantitative data are available, mean daily path length
exceeds 1200 m/day (Garber 1993).
Within the order Carnivora, there is a positive relationship
between home range size and the frequency of stereotypic
behaviour, and a positive relationship between daily path
length and the frequency of stereotypic behaviour (data
from 35 species [Clubb & Mason 2003]). Since tamarins
have considerably larger home ranges and longer daily path
lengths than marmosets, they may be more predisposed to
develop stereotypies in captivity relative to marmosets if a
similar relationship exists for the order Primates. Although
such a relationship has not been demonstrated for primates,
it is known that tamarins develop behavioural abnormalities, including stereotypies, in captive colonies (eg head
bobbing and self-inflicted trauma for S. oedipus [Box &
© 2004 Universities Federation for Animal Welfare
Rohrhuber 1993; Savage 1995]; locomotor stereotypies
[circling and weaving] and self-inflicted trauma for S. labiatus [Buchanan-Smith personal observation; Prescott personal observation]). Berkson et al (1966) report that in a
callitrichid colony of 300 animals, two were seen to perform
“cage stereotypies”; one was a black-mantled tamarin
(Saguinus nigricollis) and the other a golden lion tamarin
(Leontopithecus rosalia). Healthy marmosets kept in good
laboratory conditions seldom behave abnormally (Smith &
Boyd 2002). In a survey of UK establishments conducting
regulatory toxicology studies, marmosets were reported to
show no biting of their cages or self-inflicted trauma, and a
very low incidence of circling (0.3–1%) and weaving (1%)
(when weaving did occur it was associated with single
housing) (Hubrecht 1995).
Increasing cage size is known to reduce the incidence of
abnormal behaviour and stereotypies in primates in the laboratory, including tamarins (see Introduction). One report
shows significantly more head bobbing in pairs of S. oedipus housed in smaller cages versus larger ones (smaller
cages measured 1.0 × 0.5 × 0.7 m [= 0.35 m3] versus cages
measuring 0.9 × 0.75 × 1.7 m [= 1.15 m3] or larger [Box &
Rohrhuber 1993]). It is important to note that greater space
allowance affords more complex furnishings (which, in
turn, can increase the amount of useable space and offer
additional behavioural opportunities) without interfering
with routine laboratory husbandry (Kitchen & Martin
1996). It is widely reported that the complexity of the cage
has a clear impact on the welfare of tamarins and marmosets
(Kerl & Rothe 1996; Kitchen & Martin 1996; Gaspari et al
2000; Ventura et al 2001).
Breeding success in the laboratory
The first published reports of callitrichids being bred in captivity are from the mid-1960s (Epple 1967; Kingston 1969,
1975). C. jacchus survives and breeds well in many captive
environments, whereas other species of callitrichid do well
in some conditions but not in others (Evans 1984; Stevenson
1984, 1986; Tardif et al 1984a; Box & Hubrecht 1987). The
critical inter-specific and inter-environmental differences
remain obscure (Box 1997).
Whilst reproductive success and infant survival varies from
laboratory to laboratory, C. jacchus is now well established
in captivity. In one UK laboratory, infant survival to weaning is approaching 90% when triplet births are included
(triplets are rotationally hand-reared), although the UK
average is around 80% survival to three months (average
calculated from five UK establishments [confidential personal communication to Buchanan-Smith 2002]). Tamarins
have also been kept in laboratories for many generations
(Hampton et al 1966) but are more difficult to breed in laboratory conditions. In contrast to C. jacchus, high levels of
abortion and infant mortality (eg mean survival rate to
1 year in 10 colonies of S. oedipus is 38% [Snowdon et al
1985]) have been reported in captive colonies of S. oedipus
and S. fuscicollis (Kilborn et al 1983; Kirkwood et al 1983;
Glatston et al 1984; Snowdon et al 1985; Tardif et al 1986;
Scullion 1987; G Epple unpublished data cited in National
Cage sizes for tamarins 155
Research Council 1998 p 71). Poole et al (1999) describe
S. oedipus as being particularly prone to neglect or abandoning young following disturbance. Bardi and Petto
(2002) report that S. oedipus can experience infant mortality rates (total deaths before reaching sexual maturity) twice
as high as those of C. jacchus, despite uniformity in housing conditions and husbandry (54%, 597/1053 infants, for
S. oedipus [Bardi et al 2001]; 24%, 194/806 infants, for
C. jacchus [M Bardi & A J Petto personal communication to
Buchanan-Smith 2002]).
Tardif et al (1984a) compared the reproductive performance
of C. jacchus, S. oedipus and S. fuscicollis (mated pairs with
up to three sets of offspring) under identical housing conditions (cages measured 1.27 × 1.53 × 1.53 m = 2.97 m3).
C. jacchus was the most reliable breeder, with the lowest
percentage of stillborn infants and highest percentage of
post-weaning survival. In smaller cages (0.7 × 0.5 × 1.0 m =
0.35 m3, but allowing two of these for family groups of up
to eight members), Scullion (1987) reports that parental
neglect and attack on new-borns was common in S. oedipus.
Although few recent data are available for S. labiatus,
Ogden and Wolfe (1979) report a low incidence of live
births (only 63–71%, 32/49 infants, n = 27 deliveries, with
a 78% survival rate of live births to 1 month, n = 32) in very
small cages (0.46 × 0.46 × 0.54 m = 0.11 m3).
The well-being of primates and maximising breeding success are closely correlated (Poole et al 1999). In large enclosures, in pairs or with a group composition resembling that
found in nature, a good breeding record has been established
for S. oedipus (Brand 1981; Snowdon et al 1985; Price &
McGrew 1990). Price and McGrew (1990) report the highest survival rate for this species of 69% of infants reared by
their parents to adulthood (based on 6.5 years of records).
Mean group size for their colony was 6.9 animals housed
either in a room (2.91 × 3.45 × 3.54 m = 35.54 m3) or in two
cage units (1.97 × 1.19 × 1.68 m = 3.94 m3) with access to
an outdoor area (mean = 29.3 m3). Snowdon (1989) notes
for S. oedipus that the only colonies to report breeding success with captive born females are those with large cages,
and that infant survival increases by 50% in cage sizes of
3.0 m3 compared to 0.2 m3. Savage (1995) writes for this
species that “although variability in reproduction and infant
survival has been seen in most research colonies, the most
successful colonies have large, complex cages and animals
that have been properly socialised”. So cage size is an
important factor influencing breeding success in tamarins.
With the birth of new infants, 5 to 7 month old callitrichid
siblings become active as playmates; with the birth of
another set of infants, these animals, now juveniles
(>14 months of age), become actively involved as carriers
and caregivers (Box 1977; Ingram 1977; Cleveland &
Snowdon 1984; Snowdon 1989). This experience is very
important for the development of appropriate parental
behaviour both in marmosets and tamarins (Price &
McGrew 1990; Snowdon 1996), but it has been shown that
sibling rearing experience is more important for future
reproductive success in S. oedipus than C. jacchus (Tardif
et al 1984b). Tamarins carry and provision their infants for
a longer period than do marmosets (even after differences in
body weight are taken into account), probably because in
nature they range over larger areas (Caine 1993; Bardi &
Petto 1999). Furthermore, the presence of available helpers
and the mother’s experience affects infant viability in
S. oedipus but not in C. jacchus (Bardi & Petto 2002).
Therefore, if breeding success is to be maximised for
tamarins, it is particularly important that cages are of an
adequate size to comfortably accommodate large, naturalsized family groups long enough for older siblings to
co-operate with rearing and acquire parental competence.
Species predisposition and aggression
Aside from breeding, a main consideration in colony management of tamarins should be that animals show positive
social interactions and a minimum of overt aggression.
Under crowded colony conditions, when visual contact
between groups is allowed, tamarins display high levels of
territorial threat displays towards other visible groups
(although breeding C. jacchus with unobstructed visual
contact can also sometimes be aggressive [Ely et al 1998]).
It has been suggested that the high levels of abortion and
infant loss reported in captive colonies of S. oedipus and
S. fuscicollis are related to chronic arousal caused by the
proximity of neighbouring groups in a colony situation
(National Research Council 1998). When several tamarin
groups are housed in the same room, visual barriers placed
between adjacent cages usually appear to be sufficient to
reduce threat displays and inter-group aggressive behaviour,
even though animals in one cage can smell and hear other
groups of animals (Chamove 1989b; National Research
Council 1998). Savage (1995) reports for S. oedipus that, in
contrast to visual contact, “olfactory and auditory contact
with neighbouring groups does not cause significant disruption in behaviour and reproduction”.
Unrestricted visual contact between tamarin groups and
overcrowding can result in increased intra-group aggression
as a consequence of displaced inter-group aggression
(Savage 1995). Savage writes for S. oedipus that “the larger
the cage, the greater probability of housing large families
with minimal disruption in the group”. Approach and withdraw responses and the opportunity to produce effective
motor responses are limited in small cages. Increased cage
size may therefore help reduce intra-group aggression in
tamarins by enabling better avoidance of aggressive individuals (as is the case for macaques [Erwin 1977; Reinhardt
& Reinhardt 1991; Maninger et al 1998]).
In order to minimise both inter-group and intra-group
aggression in tamarins, and the impact these have on breeding success (Snowdon 1989), health and well-being, care
should be taken to provide them with visual barriers, and
not to overcrowd laboratory rooms with many small cages
but instead provide fewer large cages. Large cages offer
greater opportunity for enrichment, and a complex environment
reduces both inactivity and aggression in social groups of callitrichids (McKenzie et al 1986; Chamove & Anderson 1989).
Animal Welfare 2004, 13: 151-158
156 Prescott and Buchanan-Smith
Conclusions and animal welfare implications
For animals used in the laboratory, any restriction on the
extent to which they can satisfy their physical, behavioural
and social needs should be limited as far as is practicable.
Good caging is crucial in meeting this goal and should provide opportunity for exercise, permit a broad range of
species-typical behaviours, and promote appropriate social
groupings and interactions. Species-adequate housing and
husbandry are not only a safeguard for the well-being and
breeding success of laboratory animals, but also are a prerequisite for sound scientific methodology.
Adequate space alone does not in itself provide for good
welfare, but larger cages allow greater complexity of cage
furnishings. Increasing both cage size and complexity has
been shown to increase the amount of natural behaviours
and reduce the incidence and frequency of abnormal behaviours and stereotypies in many laboratory primate species.
Laboratory primates should be housed under enriched conditions that take into account their species-specific propensities and needs. If the adaptations made by these animals to
their natural environments are ignored, there is the risk of
chronic ill health and poor welfare, with the possible result
of compromising captive breeding and research.
On the basis of the literature and experience presented here,
we conclude that it is even more important to provide
tamarins with a good quantity of space in the laboratory
than it is marmosets if well-being and breeding success are
to be maximised. They should be housed in enclosures at
least as large as those specified in the UK Home Office
Code of Practice for the Housing and Care of Animals in
Designated Breeding and Supplying Establishments (Home
Office 1995) (Table 2), and preferably larger.
Acknowledgements
We gratefully acknowledge the discussion with, and advice
of, all those contacted during the writing of this paper.
Special thanks are reserved for Penny Hawkins and Maggy
Jennings who gave constructive comments on an earlier
version of this paper.
References
Alonso C and Langguth A 1989 Ecology and behavior of
Callithrix jacchus (Primates: Callitrichidae) living on an Atlantic forest island. Revista Nordestina de Biologia 6: 105-137
Bardi M and Petto A J 1999 Parental care in captive common
marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus
oedipus). American Journal of Primatology 49: 31-32 (Abstract)
Bardi M and Petto A J 2002 Parental failure in captive common
marmosets (Callithrix jacchus): a comparison with tamarins. Folia
Primatologica 73: 46-48
Bardi M, Petto A J and Lee-Parritz D E 2001 Parental failure
in captive cotton-top tamarins (Saguinus oedipus). American Journal
of Primatology 54: 159-169
Berkson G, Goodrich J and Kraft I 1966 Abnormal stereotyped
movements of marmosets. Perceptual and Motor Skills 23: 491-498
Box H O 1977 Social interactions in family groups of captive
marmosets (Callithrix jacchus). In: Kleiman D G (ed) The Biology and
Conservation of the Callitrichidae pp 239-249. Smithsonian
Institution Press: Washington, DC, USA
© 2004 Universities Federation for Animal Welfare
Box H O 1988 Behavioural responses to environmental change.
Observations on captive marmosets and tamarins. Animal
Technology 39: 9-16
Box H O 1995 Biological propensities of the Callitrichidae: a
much used — little known group. Laboratory Animals 29:
237-243
Box H O 1997 Callitrichid social biology and its significance for
captive management. In: Pryce C, Scott L and Schnell C (eds)
Marmosets and Tamarins in Biological and Biomedical Research:
Proceedings of a Workshop Organised by the European Marmoset
Research Group pp 111-118. DSSD Imagery: Salisbury, UK
Box H O and Hubrecht R C 1987 Long-term data on the
reproduction and maintenance of a colony of common marmosets (Callithrix jacchus jacchus) 1972–1983. Laboratory Animals
21: 249-260
Box H O and Rohrhuber B 1993 Differences in behaviour
among adult male, female pairs of cotton-top tamarins (Saguinus
oedipus) in different conditions of housing. Animal Technology 44: 19-30
Brand H M 1981 Husbandry and breeding of a newly established
colony of cotton-topped tamarins (Saguinus oedipus oedipus).
Laboratory Animals 15: 7-11
Bruhin H 1979 Callithrix jacchus, marmoset: new lab animal,
review. Zeitschrift Fuer Versuchstierkunde 21: 209-221
Buchanan-Smith H M 1991 A field study on the red-bellied
tamarin, Saguinus l. labiatus, in Bolivia. International Journal of
Primatology 12: 259-276
Buchanan-Smith H M 2001 Species-specific housing and husbandry for marmosets and tamarins (Callitrichinae). In: Hare V J,
Worley K E and Myers K (eds) Proceedings of the 4th International
Conference on Environmental Enrichment pp 95-105. The Shape of
Enrichment: San Diego, USA
Buchanan-Smith H M, Shand C and Morris K 2002 Cage
use and feeding height preferences of captive common marmosets
(Callithrix jacchus) in two-tier cages. Journal of Applied Animal
Welfare Science 5: 139-149
Caine N G 1993 Flexibility and co-operation as unifying themes
in Saguinus social organization and behaviour: the role of predation pressures. In: Rylands A B (ed) Marmosets and Tamarins:
Systematics, Behaviour, and Ecology pp 200-219. Oxford University
Press: Oxford, UK
Caine N G and O’Boyle V J Jr 1992 Cage design and forms of
play in red-bellied tamarins, Saguinus labiatus. Zoo Biology 11: 215-220
Caine N G, Potter MP and Mayer K E 1992 Sleeping site
selection by captive tamarins (Saguinus labiatus). Ethology 90: 63-71
Carroll J B 1997 A comparative summary of the nutritional
adaptations and needs of callitrichids and application to captive
management. In: Pryce C, Scott L and Schnell C (eds) Marmosets
and Tamarins in Biological and Biomedical Research: Proceedings of a
Workshop Organised by the European Marmoset Research Group
pp 70-77. DSSD Imagery: Salisbury, UK
Chamove A S 1989a Assessing the welfare of captive
primates — a critique. Laboratory Animal Welfare Research —
Primates: Proceedings of a Symposium Organised by Universities
Federation for Animal Welfare pp 39-49. Universities Federation for
Animal Welfare: Wheathampstead, Hertfordshire, UK
Chamove A S 1989b Environmental enrichment: a review.
Animal Technology 40: 155-178
Chamove A S and Anderson J R 1989 Examining environmental enrichment. In: Segal E F (ed) Housing, Care and Psychological
Well-being of Captive and Laboratory Primates pp 183-202. Noyes
Publications: Park Ridge, New Jersey, USA
Chamove A S and Rohrhuber B 1989 Moving callitrichid
monkeys from cages to outside areas. Zoo Biology 8: 151-163
Cage sizes for tamarins 157
Clarke J M 1994 The common marmoset, Callithrix jacchus.
ANZCCART News 7: 1-8
Cleveland J and Snowdon C T 1984 Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o.
oedipus). Animal Behaviour 32: 432-444
Clubb R and Mason G 2003 Captivity effects on wide-ranging
carnivores. Nature 425: 473-474
Council of Europe 1986 European Convention for the Protection of
Vertebrate Animals Used for Experimental and Other Scientific
Purposes, ETS No. 123. Council of Europe: Strasbourg, France
Draper W A and Bernstein I S 1963 Stereotyped behaviour
and cage size. Perceptual and Motor Skills 16: 231-234
Ely A, Freer A, Windle C and Ridley R M 1998 Assessment
of cage use by laboratory-bred common marmosets (Callithrix jacchus). Laboratory Animals 32: 427-433
Epple G 1967 Comparative investigation of the sexual and social
behavior of marmosets (Hapalidae). Folia Primatologica 7: 37-65
Erwin J 1977 Factors influencing aggressive behavior and risk of
trauma in the pigtail macaque (Macaca nemestrina). Laboratory
Animal Science 27: 541-547
European Community 1986 Council Directive 86/609/EEC on
the Approximation of Laws, Regulations and Administrative
Provisions of the Member States Regarding the Protection of
Animals Used for Experimental and Other Scientific Purposes.
Official Journal of the European Communities L358.
Evans S 1984 Captive management of marmosets and tamarins.
In: Laboratory Animal Science Association and Universities
Federation for Animal Welfare (eds) Standards in Laboratory
Animal Management pp 250-252. Universities Federation for
Animal Welfare: Wheathampstead, Hertfordshire, UK
Ferrari S F 1993 Ecological differentiation in the Callitrichidae.
In: Rylands A B (ed) Marmosets and Tamarins: Systematics,
Behaviour, and Ecology pp 314-328. Oxford University Press:
Oxford, UK
Ferrari S F and Lopes Ferrari M A 1989 A re-evaluation of
the social organization of the Callitrichidae, with reference to the
ecological differences between genera. Folia Primatologica 52: 132-147
Garber P A 1993 Feeding ecology and behaviour of the genus
Saguinus. In: Rylands A B (ed) Marmosets and Tamarins: Systematics,
Behaviour, and Ecology pp 273-295. Oxford University Press:
Oxford, UK
Gaspari F, Perretta G and Schino G 2000 Effects of different
housing systems on the behaviour of the common marmoset
(Callithrix jacchus). Folia Primatologica 71: 291
Glatston A R, Geilvoet-Soeteman E, Hora-Pecek E and
van Hooff J A R A M 1984 The influence of the zoo environment on social behavior of groups of cotton-topped tamarins
(Saguinus oedipus oedipus). Zoo Biology 3: 241-253
Hampton J K Jr, Hampton S H and Landwehr B T 1966
Observations on a successful breeding colony of the marmoset,
Oedipomidas oedipus. Folia Primatologica 4: 265-287
Hearn J P, Abbott D H, Chambers P C, Hodges J K and
Lunn S F 1978 Use of the common marmoset, Callithrix jacchus,
in reproductive research. Primates in Medicine 10: 40-49
Hershkovitz P 1977 Living New World Monkeys (Platyrrhini), with
an Introduction to Primates, Volume 1. University of Chicago Press:
Chicago, USA
Home Office 1989 Code of Practice for the Housing and Care of
Animals Used in Scientific Procedures. Her Majesty’s Stationery
Office: London, UK
Home Office 1995 Code of Practice for the Housing and Care of
Animals in Designated Breeding and Supplying Establishments. Her
Majesty’s Stationery Office: London, UK
Hubrecht R C 1985 Home-range size and use and territorial
behavior in the common marmoset, Callithrix jacchus jacchus, at
the Tapacura Field Station, Recife, Brazil. International Journal of
Primatology 6: 533-550
Hubrecht R C 1995 Housing, Husbandry and Welfare Provision for
Animals Used in Toxicology Studies: Results of a UK Questionnaire on
Current Practice (1994). Universities Federation for Animal
Welfare: Wheathampstead, Hertfordshire, UK
Ingram J C 1977 Parent–infant interactions in the common marmoset (Callithrix jacchus). In: Kleiman D G (ed) The Biology and
Conservation of the Callitrichidae pp 281-297. Smithsonian
Institution Press: Washington, DC, USA
Institute of Laboratory Animal Resources 1996 Guide for
the Care and Use of Laboratory Animals. National Academy Press:
Washington, DC, USA
International Primatological Society 1993 IPS International
guidelines for the acquisition, care and breeding of nonhuman primates. Primate Report 35 (Special issue)
Izawa K 1975 Foods and feeding behavior of monkeys in the
upper Amazon basin. Primates 16: 295-316
Kerl J and Rothe H 1996 Influence of cage size and cage equipment on physiology and behavior of common marmosets
(Callithrix jacchus). Laboratory Primate Newsletter 35: 10-13
Kilborn J A, Sehgal P, Johnson L D, Beland M and
Bronson R T 1983 A retrospective study of infant mortality of
cotton-top tamarins (Saguinus oedipus) in captive breeding.
Laboratory Animal Science 33: 168-171
Kingston W R 1969 Marmosets and tamarins. Laboratory Animal
Handbooks 4: 243-250
Kingston W R 1975 The breeding of endangered species of marmosets and tamarins. In: Martin R D (ed) Breeding Endangered
Species in Captivity pp 213-222. Academic Press: London, UK
Kirkwood J K, Epstein M A and Terlecki A J 1983 Factors
influencing population growth of a colony of cotton-top tamarins.
Laboratory Animals 17: 35-41
Kirkwood J K and Stathatos K 1992 Biology, Rearing, and Care
of Young Primates. Oxford University Press: Oxford, UK
Kitchen A M and Martin A A 1996 The effects of cage size and
complexity on the behaviour of captive common marmosets,
Callithrix jacchus jacchus. Laboratory Animals 30: 317-326
Maier W, Alonso C and Langguth A 1982 Field observations on
Callithrix jacchus jacchus L. Zeitschrift Fuer Saeugetierkunde 47: 334-346
Maninger N, Kim J H and Ruppenthal G C 1998 The presence
of visual barriers decreases agonism in group housed pigtail macaques
(Macaca nemestrina). American Journal of Primatology 45: 193-194
McGrew W C and Webster J 1995 Birth seasonality in cotton-top tamarins (Saguinus oedipus) despite constant food supply
and body weight. Primates 36: 241-248
McKenzie S M, Chamove A S and Feistner A T C 1986
Floor-coverings and hanging screens alter arboreal monkey
behaviour. Zoo Biology 5: 339-348
Molzen E M and French J A 1989 The problems of foraging in
captive callitrichid primates: behavioral time budgets and foraging
skills. In: Segal E F (ed) Housing, Care and Psychological Well-being of
Captive and Laboratory Primates pp 89-101. Noyes Publications:
Park Ridge, New Jersey, USA
National Research Council 1998 The Psychological Well-Being of
Nonhuman Primates: A Report of the Committee on Well-Being of
Nonhuman Primates. National Academy Press: Washington, DC, USA
Neyman P F 1977 Aspects of the ecology and social organization of free-ranging cotton-top tamarins (Saguinus oedipus) and the
conservation status of the species. In: Kleiman D G (ed) The
Biology and Conservation of the Callitrichidae pp 39-71. Smithsonian
Institution Press: Washington, DC, USA
Animal Welfare 2004, 13: 151-158
158 Prescott and Buchanan-Smith
Neyman P F 1980 Ecology and social organization of the cotton-top
tamarin. PhD Thesis, University of California, Berkeley, USA
Ogden J D and Wolfe L G 1979 Reproduction of wild-caught
marmosets (Saguinus labiatus labiatus) under laboratory conditions. Laboratory Animal Science 29: 545-546
Paulk H H, Dienske H and Ribbens L G 1977 Abnormal
behavior in relation to cage size in rhesus monkeys. Journal of
Abnormal Psychology 86: 87-92
Peres C A 1992 Consequences of joint-territoriality in a mixedspecies group of tamarin monkeys. Behaviour 123: 220-246
Pook A G and Pook G 1982 Polyspecific association between
Saguinus fuscicollis, Saguinus labiatus, Callimico goeldii and other primates in north-western Bolivia. Folia Primatologica 38: 196-216
Poole T B 1988 Normal and abnormal behaviour in captive primates. Primate Report 22: 3-12
Poole T B and Evans R G 1982 Reproduction, infant survival
and productivity of a colony of common marmosets (Callithrix jacchus jacchus). Laboratory Animals 16: 88-97
Poole T B, Costa P, Netto W J, Schwartz K, Wechsler B
and Whittaker D 1994 Non-human primates. In: O’Donoghue
P N (ed) The Accommodation of Laboratory Animals in Accordance
with Animal Welfare Requirements. Proceedings of an International
Workshop held at Bundesgesundheitsamt, Berlin, 17–19th May 1993
pp 81-86. Bundesministerium für Ernährung, Landwirtshaft und
Forsten: Bonn, Germany
Poole T, Hubrecht R and Kirkwood J K 1999 Marmosets and
tamarins. In: Poole T and English P (eds) The UFAW Handbook on
the Care and Management of Laboratory Animals, 7th Edition, Volume
1: Terrestrial Vertebrates pp 559-573. Blackwell Science: Oxford, UK
Poole T and Thomas A W 1995 Primate Vaccine Evaluation
Network: Recommendations, Guidelines and Information for Biomedical
Research Involving Non-Human Primates with Emphasis on Health
Problems of Developing Countries. European Commission DG-XII:
Brussels, Belgium
Prescott M J and Buchanan-Smith H M 2002 Predation sensitive foraging in captive tamarins. In: Miller L (ed) Eat or Be Eaten:
Predation Sensitive Foraging Among Primates pp 44-57. Cambridge
University Press: Cambridge, UK
Price E C and McGrew W C 1990 Cotton-top tamarins
(Saguinus (o.) oedipus) in a semi-naturalistic captive colony.
American Journal of Primatology 20: 1-12
Reinhardt V and Reinhardt A 1991 Impact of a privacy panel
on the behaviour of caged female rhesus monkeys living in pairs.
Journal of Experimental Animal Science 34: 55-58
Reinhardt V and Reinhardt A 2001 Legal space requirement
stipulations for animals in the laboratory: are they adequate?
Journal of Applied Animal Welfare Science 4: 143-149
Ross C 1988 The intrinsic rate of natural increase and reproductive effort in primates. Journal of Zoology 214: 199-219
Royal Society/Universities Federation for Animal Welfare
1987 Guidelines on the Care of Laboratory Animals and their Use for
Scientific Purposes: I. Housing and Care. The Royal Society and the
Universities Federation for Animal Welfare: London, UK
Savage A 1990 The reproductive biology of the cotton-top
tamarin (Saguinus oedipus oedipus) in Colombia. Dissertation
Abstracts International B51(4)
Savage A 1995 The Cotton-Top Tamarin SSP Husbandry Manual.
Available at: http://www.csew.com/cottontop/
Savage A, Giraldo L H, Blumer E S, Soto L H, Burger W
and Snowdon C T 1993 Field techniques for monitoring cotton-top tamarins (Saguinus oedipus oedipus) in Colombia. American
Journal of Primatology 31: 189-196
© 2004 Universities Federation for Animal Welfare
Scanlon C E, Chalmers N R and Monteiro da Cruz M A O
1989 Home range use and the exploitation of gum in the marmoset
Callithrix jacchus jacchus. International Journal of Primatology 10: 123-136
Schoenfeld D 1989 Effects of environmental impoverishment on
the social behavior of marmosets (Callithrix jacchus). American
Journal of Primatology (Supplement 1): 45-51
Scullion F T 1987 Husbandry, breeding and maintenance of a
viable population of cotton-top tamarins (S. o. oedipus) Animal
Technology 38: 167-174
Smith J A and Boyd K M 2002 The Boyd Group Papers on the
Use of Non-Human Primates in Research and Testing. The British
Psychological Society: Leicester, UK
Snowdon C T 1989 The successful captive breeding of endangered primates. In: Seth P K and Seth S (eds) Perspectives in Primate
Biology, Volume 3 pp 245-255. Today and Tomorrow’s Printers and
Publishers: New Delhi, India
Snowdon C T 1996 Infant care in cooperatively breeding
species. Advances in the Study of Behavior 25: 643-689
Snowdon C T and Savage A 1989 Psychological well-being of
captive primates: general considerations and examples from callitrichids. In: Segal E F (ed) Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates pp 75-88. Noyes
Publications: Park Ridge, New Jersey, USA
Snowdon C T, Savage A and McConnell P B 1985 A breeding colony of cotton-top tamarins (Saguinus oedipus). Laboratory
Animal Science 35: 477-480
Snowdon C T and Soini P 1988 The tamarins, genus Saguinus.
In: Mittermeier R A, Rylands A B, Coimbra-Filho A F and da
Fonseca G A B (eds) Ecology and Behavior of Neotropical Primates,
Volume 2 pp 223-298. World Wildlife Fund: Washington, DC, USA
Stevenson M F 1984 The captive breeding of marmosets and
tamarins. Proceedings of the Symposium of the Association of British
Wild Animal Keepers 8: 49-60
Stevenson M F 1986 Captive breeding of callitrichids: a comparison of reproduction and propagation in different species. In: Else
J G and Lee P C (eds) Primate Ecology and Conservation pp 301-313.
Cambridge University Press: Cambridge, UK
Stevenson M F and Rylands A B 1988 The marmosets, genus
Callithrix. In: Mittermeier R A, Rylands A B, Coimbra-Filho A F and
da Fonseca G A B (eds) Ecology and Behavior of Neotropical Primates,
Volume 2 pp 131-222. World Wildlife Fund: Washington, DC, USA
Tardif S D, Carson R L and Clapp N K 1986 Breeding performance of captive-born cottontop tamarin (Saguinus oedipus)
females: proposed explanations for colony differences. American
Journal of Primatology 11: 271-275
Tardif S D, Richter C B and Carson R L 1984a Reproductive
performance of three species of Callitrichidae. Laboratory Animal
Science 34: 272-275
Tardif S D, Richter C B and Carson R L 1984b Effects of sibling-rearing experience on future reproductive success in two
species of Callitrichidae. American Journal of Primatology 6: 377-380
Terborgh J 1983 Five New World Primates: A Study in Comparative
Ecology. Princeton University Press: Princeton, New Jersey, USA
Ventura R, Buchanan-Smith H M and Morris K 2001 An
enriched environment accelerates infant development in common
marmosets. Primate Eye 73: 19
Woodbeck T and Reinhardt V 1991 Perch use by Macaca mulatta in relation to cage location. Laboratory Primate Newsletter 30: 11-12
Yoneda M 1981 Ecological studies of Saguinus fuscicollis and
Saguinus labiatus with reference to habitat segregation and height
preference. Kyoto University Overseas Research Reports of New
World Monkeys 2: 43-50