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CALLITRICHIDS: MONOGAMY AND FAMILY LIFE
Int. Zoo Yb. (2012) 46: 109–122 DOI:10.1111/j.1748-1090.2012.00176.x
Monogamy and family life in callitrichid monkeys: deviations, social dynamics and captive management* G. ANZENBERGER1 & B. FALK2 Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland, and 2Wildtier Schweiz, Strickhofstrasse 39, CH-8057 Zürich, Switzerland E-mail:
[email protected] 1
Marmosets, tamarins and Goeldi’s monkeys Callimico goeldii (Callitrichidae) are well represented in zoos. Owing to their small size, their attractive appearance and their social organization in family groups along with extensive alloparental care, these clawed New World monkeys make fine contributions to any primate collection. In the wild, callitrichids became famous for their so-called ‘social flexibility’, whereas in captivity they can only be kept in heterosexual pairs or grown family groups. This contradiction is addressed in this article. Based on proximate aspects of behaviour, it is concluded that monogamy is the modal social grouping of any callitrichid taxon. In captive family groups of callitrichids, the underlying behavioural mechanisms that ensure the social and sexual integrity of that taxonspecific pattern give rise to the kind of social dynamics that zoo personnel have to cope with at regular intervals; that is, marked intra-group aggression and expulsion of group members. In summary, the overall behavioural theme of naturally grown groups of marmosets, tamarins and Goeldi’s monkeys seems to be that their members are torn between cooperation and competition, resulting in occasional periods of social instability. Key-words: Callitrichidae; inbreeding avoidance; intra-sexual aggression; helper system; paternal care; social dynamics; social monogamy.
INTRODUCTION Callitrichids in zoos Marmosets, tamarins and Goeldi’s monkeys Callimico goeldii (Callitrichidae) together constitute a very intriguing and interesting
taxon of the order Primates. Because of quite diverse aspects of their biology, these monkeys satisfy zoo visitors and zoo personnel at the same time. Zoo visitors are fascinated by the often colourful and sometimes bizarre appearance of callitrichids. Their social life in full families is quite special and regular twin births in marmosets and tamarins, often twice a year, result in groups showing entertaining and rich behavioural repertoires. Occasionally, all this might even be observed at close proximity under semifree-ranging conditions (see also Price et al., 2012). Because of their small body size, callitrichids can be maintained within attractive, naturally equipped and relatively large enclosures, which is popular with zoo personnel. Even mixed-species exhibits with larger New World monkey species are possible (see also Buchanan-Smith, 2012). In addition, in most cases the husbandry of callitrichids is not too complicated and breeding is not too difficult to achieve. For more detailed information two seminal volumes on keeping callitrichids in zoological gardens may be consulted, each covering a wide range of topics on housing, husbandry, social management, mixed-species enclosures, handrearing protocols, nutrition and veterinary care (Sodaro & Saunders, 1999; Bairrão Ruivo, 2010).
*This paper is dedicated to Wolfgang Wickler on the occasion of his 80th birthday.
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Plate 1. Pair of Pygmy marmosets Cebuella pygmaea plus 3 week-old twins. This photograph depicts in an eye-catching fashion the intimate tie between pair-mates, which is the basis and guarantee of any breeding success. One cannot distinguish the two sexes, nor does the individual carrying the infants provide any indication: it could equally well be 웨 or 웧. Such bound and determined cooperation permits the successful rearing of twins while the 웨 is most likely pregnant again. Norbert Steffan.
It is worth mentioning that research on callitrichids, foremost the development of selfsustaining captive colonies, is an excellent example of how universities contributed significantly to how callitrichids are managed in zoos today. This fact is vividly illustrated by authors and affiliations in The Biology and Conservation of the Callitrichidae, edited by Kleiman (1977a), as well as the Biology and Behaviour of Marmosets by Rothe et al. (1978). More recent volumes report on the continued and clearly ongoing combined efforts by zoos and universities to take forward our knowledge about callitrichid biology (Rylands, 1993; Ford et al., 2009). Characteristics of callitrichids Current taxonomies distinguish seven genera of clawed New World monkeys (Callitrichidae), namely Cebuella, Callithrix, Mico, Callibella, Saguinus, Leontopithecus and Callimico (see also Rylands et al., 2012). Apart from Callibella all of these can regularly be seen in zoos. All taxa share dwarfism as a derived character and – with the sole exception of Callimico – all show twinning
(Martin, 2012). In addition, all taxa exhibit the following morphological and social characteristics: (1) no obvious sexual dimorphism in size and appearance (Kleiman, 1977b) (Plate 1); (2) predilection towards social monogamy, based on comparable amounts of intra-sexual aggression in 웧웧 and 웨웨 (Anzenberger, 1992); (3) reduction in behavioural – and to some extent even endocrinological – dimorphism, reflected by direct paternal care (Kleiman, 1977b; Schradin & Anzenberger, 2001a,b), in parallel with elevated levels of prolactin in 웧웧 (Ziegler et al., 1996; Schradin & Anzenberger, 1999, 2004; Ziegler, 2000; Schradin et al., 2003); (4) 웨웨 show, in contrast to all other primate taxa, a post-partum oestrus resulting in relatively short inter-birth intervals and, accordingly, have a high reproductive output (Martin, 1992; Buchanan-Smith & Carroll, 2010); (5) the initial heterosexual pair grows into a family group, where older offspring help in the rearing of the younger progeny, representing a well-developed helper system and categorizing callitrichids as ‘cooperative breeders’ (Garber, 1997); (6) the parents hold the reproductive monopoly (i.e. offspring,
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even when sexually mature, do not reproduce as long as they stay in their natal group, reflecting pronounced avoidance of inbreeding among close kin) (Abbott et al., 1993; Buchanan-Smith & Carroll, 2010). A reproductive peculiarity connected with the obligatory twinning in marmosets and tamarins should be mentioned here. Callitrichid twins are somatic chimaeras (Wislocki, 1939; Benirschke et al., 1962). Accordingly, genotyping using blood DNA profiles does not make it possible to distinguish intrauterine siblings (Dixson et al., 1988, 1992). Individual-specific DNA fingerprints can only be produced when using tissues poor in leukocytes (Signer et al., 2000). Haig (1999), in a stunning theoretical paper, pointed out that chimaerism could help to explain the evolution of alloparental care and sexual suppression in callitrichids, a topic that has been corroborated by studies on Wied’s marmosets Callithrix kuhlii (Ross et al., 2007). However, behavioural genetics will not be expanded upon in this review. The six characteristics listed earlier, which partially overlap, result in three ‘syndromes’ of callitrichid biology, namely ‘monomorphism and monogamy’ (1, 2, 3), ‘bi-parental care and cooperative breeding’ (3, 4, 5) and ‘family life and inbreeding avoidance’ (5, 6). The three syndromes, and especially their intertwined proximate and ultimate relationships, will be addressed in the following account.
SOCIAL MONOGAMY Social monogamy and family groups When looking at socially monogamous mammal species, beginning with the heterosexual pair, there are two possible routes or types of grouping patterns. In both cases, family groups grow from and around the initial pairs and differ – at first sight – only with respect to species-specific mean sizes (‘nuclear family’ or ‘extended family’ sensu Kleiman, 1980). Nuclear families are composed of only a few members, such as parents and solely immature offspring, as
represented among primates by titi monkeys (Callicebus), owl monkeys (Aotus), and gibbons and siamangs (Hylobatidae). Extended families can grow much larger and contain parents and offspring of all age classes, as in Callitrichidae. It follows that in those species in which offspring do not leave the group at the time of sexual maturity, either on their own, when forced by parents or by a combination thereof, other mature individuals will be part of the group in addition to the breeding pair. In general, for the existence of social monogamy, the most immediate and also most effective behavioural mechanism is pronounced intra-sexual aggression of mature 웧웧 and 웨웨 towards unfamiliar adult conspecifics. We might assume that a comparable mechanism must be at work within family groups as well, although kin selection and possible effects of inbreeding will certainly have modifying influences as soon as offspring are concerned as competitors. However, in both situations, the overall proximate goal of intra-sexual incompatibility – towards unfamiliar as well as towards familiar conspecifics – is the social and sexual integrity of the initial pair. Whereas that is achieved by overt aggression towards unfamiliar conspecifics, within family groups it can be ensured either by more subtle dominance behaviours of the parents (intervening or suppressive behaviours) and/or result from general subordinate behaviours of the progeny (submissive or inhibited behaviours). The most remarkable biological phenomenon in this connection is the sexual suppression or inhibition of 웨 offspring in callitrichids. This may be controlled only at the behavioural level but it may even give rise to complete ovarian inactivity and infertility as long as 웨웨 remain in their natal group (Abbott et al., 1993). Parent–offspring relations can be well balanced for quite long periods. However, the costs of ‘paying for staying’ (Kokko et al., 2001) for offspring increase gradually as they age, finally culminating at a point where compatibility between parent and offspring no longer exists and social conflict in family
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groups becomes insurmountable (see Social Dynamics later). Social monogamy and intra-sexual aggression In most callitrichid species it can be assumed that there is a bias towards a stronger intra-sexual aggression in 웨웨 than in 웧웧 (for evidence in captivity: Epple, 1975; Kleiman, 1979; French & Inglett, 1989). This assumption rests on the fact that 웧 help in infant care mirrors the extreme reproductive burden borne by the 웨, namely nursing twins and being pregnant with the next set of infants. Accordingly, direct paternal assistance eases the maternal burden (Schradin & Anzenberger, 2001b) and seems to be ultimately connected to the evolution of twinning and post-partum oestrus in callitrichids (Dunbar, 1988). It follows that 웧웧, as sorely needed helpers for infant care, represent for 웨웨 a resource that has to be defended. There is one callitrichid species that underpins that reasonable interpretation: Goeldi’s monkey Callim. goeldii. Callimico mothers carry their (single) offspring much longer than mothers of other callitrichid species and show the capacity – at least for the first 3–4 weeks post-partum – to care for the infant on their own (Schradin & Anzenberger, 2003). Obviously, 웨 Goeldi’s monkeys are less dependent on 웧웧 as helpers and exhibit less intra-sexual aggression than 웧웧 (pers. obs). In addition, Callimico is a slightly dimorphic species in comparison to other callitrichids, for its sternal glands show a clear-cut difference between mature 웧웧 and 웨웨. A histological study of sternal glands in Callimico (Rudolf von Rohr, 2005; G. Anzenberger, C. Rudolf von Rohr & T. Heinzeller, unpubl. data) revealed – taking size and morphology of the glands as indicators of function and/or scent-marking capability – that 웧웧 must be much more active and effective than 웨웨. We might speculate that such morphological and behavioural gender differences could provide some potential for polygyny in this species. That is, in fact, indicated both by anecdotal
evidence from the wild (Porter, 2007) and by an experimental study of polygynous Callimico trios in captivity (Mattle et al., 2008). However, these potential social deviations do not necessarily rule out social monogamy as the modal grouping pattern of Callimico too, and it is not recommended to keep this species in polygynous groups in captivity (Carroll, 1988). There is a convincing correlation between social structure (including mating system) and morphological differences between the sexes that can be reduced to the following rule: monogamous species do not show differences in body size or canine size, whereas those differences are often pronounced in polygynous species (Harvey & Harcourt, 1984; Willner & Martin, 1985; CluttonBrock, 1991). Returning to the previous statement that in callitrichids 웧웧 are needed to assist in infant care, and linking it to the existing helper system of callitrichids (cooperative breeding), polyandry is the logical and only social alternative when it comes to possible deviations from monogamy (Fig. 1). In fact, that kind of social grouping has been shown for some callitrichid species in the wild; for example, Tassel-ear marmoset Callithrix humeralifer (Rylands, 1986), Saddleback tamarin Saguinus fuscicollis (Goldizen, 1987), Moustached tamarin Saguinus mystax (Huck et al., 2005) and Geoffroy’s tamarin Saguinus geoffroyi (Diaz-Munoz, 2011). There are two rules of thumb regarding callitrichid social systems. First, although several adults of both sexes may be encountered in particular groups, usually only one 웨 reproduces (Ferrari & Digby, 1996; Garber, 1997). Second, if more than one 웧 copulates with the breeding 웨 in a group, behavioural monopolization by the dominant 웧 becomes evident (e.g. for wild Golden lion tamarins Leontopithecus rosalia see Baker et al., 1993). This pronounced mate-guarding behaviour seems to be typical for callitrichids (Anzenberger, 1992) and recently these behavioural findings have been supported by genetic data from two wild ‘polyandrous’ callitrichid species, namely the Moustached tamarin S. mystax (Huck et al., 2005) and
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female needs male help
female intra-sexual intolerance
care for twin infants
social polyandry
male profits from additional help
male intra-sexual tolerance
Fig. 1. Flow chart illustrating ultimate and proximate aspects for polyandry as a social deviation from monogamy in marmosets and tamarins. Essential features of the reproductive biology of marmosets and tamarins are summarized and it is assumed that both taxa exhibit social monogamy as their modal grouping pattern. However, if deviations occur, they should lead to polyandry rather than to any other social grouping. This prediction assumes that litter size would determine the extent of cooperation for breeding, which in turn brings about sex-specific social tendencies leading to only one 웨 but allowing more than one 웧.
the Geoffroy’s tamarin S. geoffroyi (DiazMunoz, 2011). In groups containing multiple adult 웧웧, which were observed mating with the breeding 웨, paternity was nevertheless restricted – with very few exceptions – to just the dominant 웧. One more aspect needs to be stressed. Ferrari & Lopes Ferrari (1989) have proposed the following for callitrichids: ‘where polyandrous mating occurs, it will be “fraternal”, i.e. stable relationship between a single 웨 and a number of 웧 siblings.’. The results of the Diaz-Munoz (2011) report point precisely in this direction because the polyandrous 웧웧 in this study had a kinship value consistent with fraternal (or filial) relationships and they could also share paternity. That polyandry must be regarded as a deviation from monogamy is underlined by the fact that testis sizes in polyandrous callitrichid species fall right among the values for monogamous species. In other words, there are absolutely no indications that 웧웧 of polyandrous callitrichid species have been selected for sperm competition as is clearly visible in 웧웧 of species living in multi-웧/ multi-웨 groups (Harvey & Harcourt, 1984; Willner & Martin, 1985). In other words, the strong correlation between testis size and social structure holds for callitrichid species as well. Males living in polyandrous mating systems seem to benefit, through higher intra-sexual compatibility, from – at least – occasionally shared paternities.
Additional genetic data for wild callitrichids are available only for one other species, the Common marmoset Callithrix jacchus. Results to date indicate groups of close kin or family groups with occasional immigrants (Dixson et al., 1992; Nievergelt et al., 2000), and are hence in full agreement with the social term ‘stable extended families’, coined for Callithrix groups by Ferrari & Digby (1996). However, based on a study using mitochondrial DNA, Faulkes et al. (2003) found multiple matrilines in some wild groups of Common marmosets. Social monogamy and dispersal pattern For polygamously living mammals there is a general tendency for the 웧웧 to leave the natal group (Greenwood, 1980). Male emigrants have one of two species-specific social alternatives: (1) 웧웧 join a 웧 bachelor group where they undergo further ontogenetic and social developmental steps that are prerequisites for acquiring 웨웨 later on; (2) 웧웧 directly join a new multi-웧/multi-웨 group where they can eventually achieve reproductive status. There are exceptions to this usual pattern of 웧 dispersal in mammals in which the 웨웨 change groups instead (for primates see: Moore, 1984; Strier, 1994). At first sight, there are no obvious features common to all of the few mammalian taxa in which 웨 emigration occurs. However, Clutton-Brock
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(1989) concluded from a comparative study that the common denominator for all of them seems to be that the effective breeding tenure of 웧웧 exceeds the age of 웨웨 at first conception. In such cases, 웨웨 emigrating from their natal groups avoid the risk of inbreeding with their fathers or other close relatives, which is probably the driving selective pressure. It is remarkable that two striking facts of mammalian social life have been only rarely addressed hitherto. First, there has not been a single report of 웨 bachelor groups for any species. Second, bachelor groups – be they 웧 or 웨 – have never been reported for any socially monogamous species. The latter fact reveals that in monogamous species dispersal patterns are obviously balanced; that is, both sexes must leave their natal groups to the same extent. However, although no sexbiased dispersal pattern seems to exist in monogamous species, it is possible that prevailing demographic conditions in a group might create pressures that – for a specific short period of time – may act more strongly on one sex than on the other. Following emigration from the natal group, individuals of both sexes have three options. They may live singly for a while, or meet and pair up with an opposite-sexed conspecific with the same social history, or – depending on rare breeding vacancies – immigrate into an existing group (see later for demographic constraints of this situation). The very few reports of dispersal pattern and formation of new groups in callitrichids, namely for Buffyheaded marmosets Callithrix flaviceps, state that members of this taxon may emigrate as same-sexed sibling pairs or trios (Ferrari & Lopes Ferrari, 1989; Ferrari & Diego, 1992). For case studies on dispersal movements in connection with the opening of breeding vacancies in wild Common marmosets Callit. jacchus see Lazaro-Perea et al. (2000). Savage et al. (1996) presented data for wild Cotton-top tamarins Saguinus oedipus on demography, group compositions and dispersal over a period of 5 years, and elaborated a model of the reproductive strategies 웨웨 and 웧웧 could opt for during dispersal events.
Incongruity between field and captive studies in callitrichids Marmosets, tamarins and Goeldi’s monkeys were first systematically studied in captivity (Epple, 1975; Rothe et al., 1978). From these studies on representatives of different genera it was evident that these monkeys could be kept only in heterosexual pairs or in groups stemming from such pairs. Any kind of polygamous association established with unfamiliar individuals turned out to be relatively unstable socially and often resulted in injury or even death. Accordingly, the logical conclusion was that the normal social grouping of callitrichids must be of a monogamous nature. From the mid-1970s onwards, callitrichids were also studied for extensive periods in the wild (see Kleiman, 1977a). Soon afterwards, based on these field data, the findings from studies in captivity were questioned. One major consequence was that the monogamous lifestyle of callitrichids was regarded as an artefact of captivity. Subsequently, the so-called ‘social flexibility’ of callitrichids became prominent in publications (e.g. Goldizen, 1988) and an entire array of social groupings from polyandry to polygyny and all possible combinations thereof were reported. In addition, the assumption of family groups was questioned and high rates of turnover between groups – through the exchange of group members – became regarded as the rule rather than the exception (Dawson, 1977; Neyman, 1977; Scanlon et al., 1988). These contradictory findings resulting from work conducted in captivity versus observations carried out in the wild are puzzling and need to be addressed. If we delve back into the history of studies on wild callitrichids, it emerges that the first attempts involved highly disturbed, manipulated or translocated populations. Dawson (1977) studied behavioural ecology of a population of Panamian Geoffroy’s tamarins Saguinus (oedipus) geoffroyi from which, for a parallel study on reproductive parameters, five individuals were culled every other week over the
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course of a year, totalling 131 individuals (Dawson & Dukelow, 1976). Neyman (1977) studied free-living Cotton-top tamarins S. oedipus and, for purposes of locating the groups, animals were equipped with bells around their necks. Garber et al. (1984) conducted a study on a population of Moustached tamarins S. mystax that had been captured on the mainland and transferred to an island (Padre Isla). For this study 20 tamarin groups, a total of 87 individuals, were trapped and animals trapped together were fitted with same-coloured collars before releasing them on the island. Some time later, encounters with island groups containing members with differently coloured collars were translated into ‘a significant amount of immigration/emigration had occurred in the groups’. In a study on wild Common marmosets, group membership was inferred only by the capture-recapture method with no intervening behavioural observations for extensive periods (Scanlon et al., 1988). Given the demanding working conditions in the field, it is not our intent to criticize those studies and we acknowledge that times as well as topics of research might have been different. However, it is difficult to understand why those studies provided a basis for questioning the findings of carefully conducted investigations of captive callitrichids. Sussman & Kinzey (1984), for example, stated ‘in large part, the study of family groups in the laboratory has led to (these) misconceptions, since long-term field studies have not supported the laboratory findings’. Such conclusions may be partly attributed to the fallacy that data from field studies are often regarded as yielding superior evidence compared to captive studies, because they deal with natural behaviours. In this connection, a general word of caution is appropriate: behaviours shown under captive conditions are by no means ‘un-natural behaviours’ but adaptive behaviours, contained in the species’ ethogram and shown in response to an admittedly special and altered kind of environment. In sum, it seems that early studies on wild callitrichids, and especially the subsequent reviews thereof, somehow ignored three fundamental points.
1. Such studies and subsequent reviews overlooked the evolutionary implications of the monomorphic character of all callitrichid species. First, there is a convincing correlation between sexual dimorphism and social structure and, second, mammalian monogamy goes along with the formation of family groups, nuclear or extended. Although a few exceptions exist, one may speculate that the fact that this grouping pattern can be observed across such different taxa as beavers, dwarf antelopes, meerkats, dwarf mongooses, bush dogs, wolves and wild dogs points towards an evolutionary principle. One might even speculate that the proximate causation of grouping tendencies would appear to be as species-specific as morphological features and restrict social flexibility to a remarkable extent. 2. In behavioural biology it is essential to differentiate between social system and mating system. However, both terms are descriptive, both rest on behavioural observations and, as such, both are equally meaningful. The term ‘mating system’ can only provide convincing biological evidence when its behavioural consequences are rendered visible; that is, the genetic outcome of the sexual relationships observed. Unfortunately such genetic data did not exist for the early studies on wild callitrichids and have become available only recently (e.g. Huck et al., 2005; Diaz-Munoz, 2011). 3. Studying wild groups of any animal species at any given point of time lacks the history of the group. That is to say, the researcher might be able to reconstruct the social situation to some extent but usually the past and genesis of a group remain completely hidden. This can be illustrated by demographic events following immigration of an unfamiliar animal into a group after the loss of one of the breeding individuals. In general, no monogamously paired individual will remain single after the loss of its mate but will seek a new one. It then depends on the demographic composition of the group, such as the age and sex of the offspring still present with the single parent, whether a stranger can move into the group
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without problems or whether the group will fall apart owing to ongoing aggression between older offspring and the same-sexed new arrival (see Social Dynamics). In a case study on captive Common marmosets Callit. jacchus, an unfamiliar 웧 was introduced to a widowed 웨 together with her four adult daughters (Kirkpatrick-Tanner, 1998). The 웨 group had been under systematic observation starting 3 months before the introduction of the strange 웧 and the subsequent events of social dynamics – both behavioural and endocrinological – were monitored in great detail. At the time of introduction of the unfamiliar 웧, the mother and two of her daughters were cycling. These findings indicate two facts: first, the subdominant 웨웨 – after the death of the father – underwent an endocrinological emancipation, although the mother was still present; second, the three 웨웨 concerned (mother and two daughters) now found themselves in a context of sexual competitors. Notwithstanding the fact that we are dealing with a case study in captivity, the social dynamics – covering a period of 1·5 years – seem to reflect the likely situation in the wild quite well (e.g. LazaroPerea et al., 2000): several 웨웨 gave birth, 웨 infanticides occurred (Kirkpatrick-Tanner et al., 1996) but some offspring survived. Several adult 웨웨 were evicted either by the mother, a daughter or a sister, and only after 17 months the group once again consisted of a monogamous pair and a few subadults (Kirkpatrick-Tanner, 1998). This example vividly illustrates so-called ‘social flexibility’. Observations would have simply depended on the stage of the group’s history at which a researcher arrived and any composition from polygyny to monogamy could have been seen. In addition, if genetic tests had been performed, it would have emerged that ‘offspring’ were related either to the 웧 or to the 웨 (with r = 0·25–0·5) or to both of them, leading to speculations about social turnover. In reality, one would have witnessed no more than the transient reconstitution events of a group (initially a monogamous pair plus its offspring) follow-
ing the death of the breeding 웧 and the subsequent immigration of an unfamiliar 웧.
SOCIAL DYNAMICS Intra-group aggression and expulsions of group members Nowadays, breeding of callitrichid species does not pose any major problems for zoos. As long as the nutritional demands are met and, especially, the vitamin D3 needs are respected (Martin, 2012), marmosets, tamarins and Goeldi’s monkeys – with very few exceptions – reproduce relatively easy. However, this also creates challenges for husbandry and captive care. As all callitrichids but Goeldi’s monkeys are twinning species and have the potential to produce and rear two litters per year, a group of about six will exist 1 year after an initial pair has been established. As soon as groups become about twice as large, after about 3 years have elapsed, social dynamics begin to come into play and some individuals are expelled from the group, often at quite regular intervals. More than ten individuals in a group also means that the oldest offspring have been sexually mature for quite some time (i.e. they may be more ‘serious’ competitors). Expulsions accompany marked intra-group aggression and can result in group members being severely injured very quickly, after which they must be removed immediately. As a consequence, larger family groups of callitrichids have the potential to keep curators and studbook keepers quite busy. It is noteworthy that in a colony of Common marmosets Callit. jacchus kept at the University of Zürich (Department of Psychology), expulsions of group members were not arbitrarily distributed across the 6 months of the regular inter-birth intervals but timely lumped. Altogether, taking data from a 12 year period and a total of nine different family groups, there were 45 evictions with 24 웧웧 and 21 웨웨 being the targets. The overall sex ratio of the offspring was balanced, as was the number of offspring per family across expulsion events. For both
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sexes, offspring were evicted significantly more often 1 month after a new birth than during the other 5 months combined (웧웧 z = 10·5, P < 0·0001; 웨웨 z = 9·8, P < 0·0001; Sign test). Our interpretation of this temporal concentration of events is the following: a new birth in a group means that the breeding 웨 enters oestrus soon afterwards. We assume that the pheromones she produces not only reach the breeding 웧 but also are detected by the older, mature offspring and hence trigger the social dynamics. In practically all cases of expulsions it is plain to see who the opponents are.As a rule of thumb, within-group aggressions are also intra-sexual aggressions. In most cases either same-sexed twin or sibling pairs or samesexed parent–offspring pairs are involved as aggressor and victim. Occasionally, at the climax of an expulsion event, all group members might participate, regardless of the sex of the victim. Whenever expulsion behaviours (threatening displays, chasing, attacks) have started, the target animal remains in focus and not even submissive behaviours will counter aggression by the dominant animal. In contrast, comparable social situations in polygamous primate species (multi-웧/ multi-웨 groups; polygynous and polyandrous groups) seem to be quite different, because here low-ranking members showing submissive behaviours may remain in the group. Moreover, the occurrence and intensity of callitrichid expulsions are not a question of the size of the enclosure but depend upon a strong proximate drive of the aggressor. The victim is actively sought out and quickly detected in any possible hiding place, and the chase is resumed. Eventually, the target individual becomes completely peripheralized and – under captive conditions – must be removed in order to preclude major injuries. In the wild, the target individual would most probably leave the group for good. When reflecting on the proximate causes for these expulsions in callitrichid species once again we encounter pronounced intrasexual incompatibilities as characteristic for any monogamous grouping. But now they are targeted at an individual’s own offspring or
kin. If one witnesses this kind of social dynamics for the first time, it is hard to believe that a group member, which was born into and lived in the group for years, is treated like an absolute stranger virtually from one minute to the next. After the initial behaviours, still at low frequencies, had occurred the development could never be halted in any of the expulsion events we witnessed in our colonies across three callitrichid genera (namely Cebuella, Callithrix and Callimico) (G. Anzenberger & B. Falk, pers. obs). At the beginning, expelled group members were kept in separated compartments of the living cage or room of the family group, with the aim of eventually reuniting the opponents. After weeks without any overt aggression at the wiremesh, as soon as the door between the compartments was opened again, the victim was immediately attacked. According to our data and colony records, expulsions of members from captive groups of Pygmy marmosets Cebuella pygmaea, Common marmosets and Goeldi’s monkeys are simply irreversible. Snowdon & Pickhard (1999) published a survey of severe aggression occurring over a 20 year history of a Cotton-top tamarin S. oedipus colony. Inglett et al. (1989) addressed this topic for a colony of Golden lion tamarins L. rosalia. By and large, results from these additional two genera seem to parallel the above-sketched pattern of intra-group aggression in captive callitrichids. However, L. rosalia seems to be different insofar as in this species expelled individuals can be reintroduced to their groups. Inglett et al. (1989) describe a protocol for a procedure that proved to be successful in almost 12 cases but all but one concerned the reintegration of 웧웧. In summary, expulsion of members occurs repeatedly with large callitrichid families. As a consequence, enclosures for callitrichid species need additional, relatively spacious compartments, which permit expelled animals to be kept separated (for a while) but still in visual, olfactory and auditory contact with the group. The expulsion events appear very dramatic under captive conditions, particularly because the victim is hindered from
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escaping by the accompanying fierce behaviours of the aggressors, which seem somewhat exaggerated as if observed through a magnifying glass. However, these events are by no means artefacts of captivity but are natural and proximately caused behaviours, which in the wild lead to the dispersal of animals and the founding of new groups.
already lived in the enclosure that will subsequently be used for the pair, it is better to put the inhabitant of the enclosure into the introduction cage and allow the newcomer to explore its new environment first.
RECOMMENDATIONS FOR CAPTIVE MANAGEMENT
The success of an introduction of an unfamiliar individual (step-parent) into an existing group depends heavily on the demographic composition of that group. In general, offspring of both sexes younger than 6 months of age (i.e. still infants; for age classes of Common marmosets as well as species differences in developmental rates see Yamamoto, 1993) cause no problems but soon accept the newcomer. However, the situation concerning maturing (c. 12 months of age) and adult offspring is quite different. Again, the characteristic intra-sexual aggression of callitrichids poses a major problem; that is, older offspring having the same sex as the step-parent will become involved in fights, either initiated by themselves or as targets. Adult opposite-sexed offspring will usually be tolerant of newcomers but often they get into quarrels or fights with the remaining parent, with which they are now in sexual competition. Accordingly, the introduction of an unfamiliar individual into an existing group will eventually result in a new pair and one or possibly two sets of offspring of one mate, stemming from its former partner. In addition, it must be stressed that inbreeding avoidance (see later) – concerning the step-parent – will be very weak as soon as these offspring reach maturity, meaning that intra-group conflicts are only postponed.
There are several social characteristics, founded in the behavioural biology of callitrichids, which have important consequences for the husbandry and management of these monkeys in captivity and which need to be addressed. The following recommendations are based on the authors’ personal observations of callitrichid behavioural biology under captive conditions. Thereby, our combined knowledge is resting – for the two named authors – on 30 years’ experience of housing Common marmosets, Pygmy marmosets and Goeldi’s monkeys as well as their social management for ethological studies. At the same time, our work covered all aspects of keeping these three species, including daily maintenance and feeding routines. We would like to stress that for further information on the following topics, noteworthy articles exist on social management of callitrichids in zoos by Baker & Savage (1999) and Buchanan-Smith & Carroll (2010). 1. Pairing of unfamiliar heterosexual individuals Owing to their monogamous predilections and the lack of sexual dimorphism (i.e. body size and strength are equal), pairing of an unfamiliar 웧 and a 웨 is always unproblematic. Normally, new mates can be introduced to each other without great precautions. However, an introduction cage prevents unexpected developments. If one or both animals have lived singly for a while, using an introduction cage is definitely recommended. Moreover, if one individual has
2. Introduction of an unfamiliar individual to an existing group
Integration of an unfamiliar male to a fatherless group Callitrichid 웧웧 seem to be very tolerant of non-genetic offspring. In our colony of Common marmosets, in a total of 12 cases, no harm, let alone fatalities, resulted when an unfamiliar 웧 was introduced to a 웨 with newborn to juvenile offspring. The hypothetical
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explanation for this is that (a) in species with post-partum oestrus an infanticide would not hasten the receptivity of the 웨, hence not heighten the 웧’s breeding success, and (b) in species with a pronounced helper system the 웧 will profit from any helper; that is, in killing the 웨’s offspring the 웧 would eliminate the first set of helpers for its own young with the 웨. Integration of an unfamiliar female to a motherless group Callitrichid 웨웨 seem to be less tolerant of unfamiliar offspring. That might be rooted in the usually higher intra-sexual intolerance in 웨웨 than in 웧웧. In practice this means that a 웨 often evicts same-sexed unfamiliar offspring at an earlier age than a 웧 step-parent would. 3. Inbreeding avoidance and non-reproductive groups Pronounced inbreeding avoidance exists in all callitrichids studied so far. However, it has been reported that in Pygmy marmosets Ce. pygmaea this phenomenon might be less developed, as indicated by occasional cases of inbreeding in captive groups (Schröpel, 1998). One explanation for this has been that the specific ecology of living in fragmented microhabitats, with little possibility for dispersal owing to high predator pressure, makes inbreeding for Pygmy marmosets into a ‘making the best of a bad job’ phenomenon. For members of the other five taxa (Callithrix, Mico, Saguinus, Leontopithecus and Callimico) the phenomenon of inbreeding avoidance seems quite uniform and strikingly convincing (Baker & Savage, 1999; Buchanan-Smith & Carroll, 2010). That means that groups in which one of the breeding individuals died may persist for years as non-reproductive units. The same holds for parent–offspring pairs as well as for brother– sister pairs. There is the possibility that, after the loss of a breeder, a group might become unstable and fall apart as a result of tensions between adult members (for Common mar-
mosets see Rothe & Darms, 1993). We might take these social dynamics as an indication that the mature members of such groups are now looking for breeding opportunities, which will not open up as long as they continue to live with close kin. One possibility to look into the inbreeding avoidance mechanism is to search studbooks as De Vleeschouwer et al. (2001) did for Golden-headed lion tamarins Leontopithecus chrysomelas. This approach is a specifically powerful test because it would be expected that in captivity inbreeding avoidance would be more easily overruled because animals are virtually unable to escape from the given social situation. The European population of L. chrysomelas contained (during the period 1984–1998) a total of 94 mature daughters that could have bred within their native groups. However, inbreeding occurred only in three intact family groups; that is, both parents present, no contraception applied to the breeding 웨 and absolutely no interruption of the continuous housing together of all family members. Similarly low figures hold for Goeldi’s monkeys, for which the first author was European Endangered Species Programme coordinator for more than a decade. Price (1998) compiled inbreeding incidents of several callitrichid species kept at the Jersey Wildlife Preservation Trust (now Durrell Wildlife Conservation Trust), Jersey, British Channel Islands. Although there have been 14 cases reported, there is only one case where inbreeding occurred in an intact family (Chaoui & Hasler-Gallusser, 1999; for one additional case in Common marmosets see Anzenberger & Simmen, 1987). This brings us to the final point that is highly relevant for both curators and studbook keepers. After a breeding animal has died in a callitrichid group, curators like to replace the loss as soon as possible in order to display a group with all age classes and a rich family life. However, because of the social dynamics illustrated above, the studbook keeper must not only find a new mate (often easy) but also has to find new places for all sexually mature offspring (practically impossible). Given that
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the inbreeding avoidance mechanism in callitrichids is almost a hundred per cent effective, the immediate solution is to leave the group as it is. Such non-reproductive groups still show a rich family life; that is, they remain attractive groups for exhibit. In addition, nonreproductive groups are very useful for the effective management of captive callitrichid populations, and no contraception is needed. In general, the numbers for most callitrichid taxa in captivity are in a good shape but at the same time there is no longer unlimited space for them in zoos. ACKNOWLEDGEMENTS We extend our grateful thanks to Bob Martin, as well as to two anonymous reviewers, for comments on earlier drafts of the manuscript, and Norbert Steffan for the use of the photograph in Plate 1.
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Manuscript submitted 6 September 2011; revised 10 February 2012; accepted 13 February 2012
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