A new male in the group: a blessing or a burden? : The role of resident female behaviour in male group entry in primates

Dispersal is widespread among the animal kingdom, and is associated with costs and benefits. For group-living animals dispersal often entails additional social costs of entering a new group. These costs may be especially apparent in primate species living in multi-male multi-female groups with male biased dispersal. Within these species, males face the challenge to obtain a new social position in a group with a cohesive core of related females, and multiple males to compete with. Up to now, researchers mainly focused on male-male competition during male group entry. However, the behavioural process accompanying integration (i.e. establishing a social position in a new group) is understudied. There is basic understanding of the behaviour of new males during group entry, but the role of resident females during male group entry has not received much attention. However, females are likely to interact with new males, based on female mate choice and the fact that new males may commit infanticide. Female tolerance may even be crucial for successful integration of new males. However, systematic studies on female behaviour during male group entry are lacking. This information is, however, critical to fully understand the social costs of male dispersal. The research described in this thesis aimed to gain better understanding of female-new male interactions during male group entry, through studying male introductions in captive naturalistic groups of rhesus macaques (Macaca mulatta) and long-tailed macaques (M. fascicularis). Interactions between resident females and new males were studied from an applied (Chapter 3-5) and fundamental (Chapter 2 and 6-8) point of view. The applied studies focussed on improving the behavioural management strategies of captive primate groups and thereby enhancing animal welfare. The studies elaborate on the effect of management and introduction procedures on introduction success, and the development of quantitative measures to determine how introductions progress and whether they may succeed. The studies show that mimicking nature closely in management procedures and during introductions increases introduction success and the long-term stability of a male’s position in the group. The fundamental studies focussed on quantifying all possible female-new male interactions, determining the fitness consequences of these interaction, and identifying which females interact with new males and why. The research showed that females can use aggression, affiliation and mating to affect the costs and benefits of male group entry, through the formation of bonds, limiting or stimulating mating access and the initiation of conflicts. Females can even prevent new males from entering a group. Factors such as infanticide risk, female reproductive state, the female’s social network and male condition may determine a female’s response to a new male. Overall, it is clear that females are active contributors to, and not passive onlookers in, the process of male group entry

A new male in the group: a blessing or a burden? : The role of resident female behaviour in male group entry in primates

Dispersal is widespread among the animal kingdom, and is associated with costs and benefits. For group-living animals dispersal often entails additional social costs of entering a new group. These costs may be especially apparent in primate species living in multi-male multi-female groups with male biased dispersal. Within these species, males face the challenge to obtain a new social position in a group with a cohesive core of related females, and multiple males to compete with. Up to now, researchers mainly focused on male-male competition during male group entry. However, the behavioural process accompanying integration (i.e. establishing a social position in a new group) is understudied. There is basic understanding of the behaviour of new males during group entry, but the role of resident females during male group entry has not received much attention. However, females are likely to interact with new males, based on female mate choice and the fact that new males may commit infanticide. Female tolerance may even be crucial for successful integration of new males. However, systematic studies on female behaviour during male group entry are lacking. This information is, however, critical to fully understand the social costs of male dispersal. The research described in this thesis aimed to gain better understanding of female-new male interactions during male group entry, through studying male introductions in captive naturalistic groups of rhesus macaques (Macaca mulatta) and long-tailed macaques (M. fascicularis). Interactions between resident females and new males were studied from an applied (Chapter 3-5) and fundamental (Chapter 2 and 6-8) point of view. The applied studies focussed on improving the behavioural management strategies of captive primate groups and thereby enhancing animal welfare. The studies elaborate on the effect of management and introduction procedures on introduction success, and the development of quantitative measures to determine how introductions progress and whether they may succeed. The studies show that mimicking nature closely in management procedures and during introductions increases introduction success and the long-term stability of a male’s position in the group. The fundamental studies focussed on quantifying all possible female-new male interactions, determining the fitness consequences of these interaction, and identifying which females interact with new males and why. The research showed that females can use aggression, affiliation and mating to affect the costs and benefits of male group entry, through the formation of bonds, limiting or stimulating mating access and the initiation of conflicts. Females can even prevent new males from entering a group. Factors such as infanticide risk, female reproductive state, the female’s social network and male condition may determine a female’s response to a new male. Overall, it is clear that females are active contributors to, and not passive onlookers in, the process of male group entry

Female social behaviour during three male introductions in captive groups of rhesus macaques

Introductions of new males into captive primate groups are often necessary to prevent inbreeding, but also bear high social risks. To minimize these risks, it is crucial to understand the social behaviour accompanying male introductions. While the behaviour of new males is generally understood, information on resident female behaviour during introductions is lacking. We studied female behaviour towards the new male during introductions of three adult male rhesus macaques (Macaca mulatta)—each into a different captive group. All three males were successfully introduced; respectively 100%, 92%, and 83% of the females tolerated the male as a group-member at the end of the introductions. Older females started tolerating the male significantly faster than younger females, while no additional effect of female dominance rank, fertility, or the number of female coalitionary partners on timing of tolerance was found. During the course of the integration, female aggression and submission towards the male, and male mating access decreased, while female affiliation towards the male increased. The increase of female tolerance and the changes in social behaviour were similar between the introductions, indicating a general pattern in female behaviour, although some variation in effect size and significance level was observed. Based on these results, we suggest that low female submission levels towards an introduced male may constitute a criterion to assess the risk of leaving the male in the group full-time. Moreover, low female aggression levels at the end of the introduction may signal long-term group stability. Overall, we conclude that female behaviour can provide valuable information about the male introduction process and should not be overlooked

Multigenerational Social Housing and Group-Rearing Enhance Female Reproductive Success in Captive Rhesus Macaques (Macaca mulatta)

To optimize costs and reproductive success, rhesus macaques in biomedical primate research facilities are often peer-reared. Older, dependent infants are typically removed from their natal group to enhance female reproduction. The minimal husbandry age-norm of infant removal is ten months. These practices deviate from species-specific behavior and may reduce welfare, suggesting a trade-off between female reproduction and welfare. However, the effect of breeding group type and rearing history on female reproductive success (i.e., birth rate; inter-birth interval (IBI); offspring survival) is unclear. This retrospective study investigated whether group type (i.e., peer groups versus multigenerational groups) and rearing history (i.e., peer-or hand-reared; group-reared with peer-or hand-reared mother; group-reared) affected female reproductive success in captive rhesus macaques. Data on female reproduction between 1996 and 2019 were collected at the Biomedical Primate Research Centre, Rijswijk. Birth rates were higher in multigenerational breeding groups than in peer groups. Moreover, group-reared females had higher offspring survival than peer-or hand-reared females. IBI was not affected by breeding group type or female rearing history. However, females in both peer and multigenerational breeding groups typically conceived earlier after giving birth than the husbandry infant removal age-norm of ten months. Thus, infant removal at an age of ten months does not enhance a female’s reproduction. Altogether, female reproduction and non-human primate welfare can simultaneously be optimized through multigenerational breeding groups and group-rearing

Female social behaviour during three male introductions in captive groups of rhesus macaques

Introductions of new males into captive primate groups are often necessary to prevent inbreeding, but also bear high social risks. To minimize these risks, it is crucial to understand the social behaviour accompanying male introductions. While the behaviour of new males is generally understood, information on resident female behaviour during introductions is lacking. We studied female behaviour towards the new male during introductions of three adult male rhesus macaques (Macaca mulatta)—each into a different captive group. All three males were successfully introduced; respectively 100%, 92%, and 83% of the females tolerated the male as a group-member at the end of the introductions. Older females started tolerating the male significantly faster than younger females, while no additional effect of female dominance rank, fertility, or the number of female coalitionary partners on timing of tolerance was found. During the course of the integration, female aggression and submission towards the male, and male mating access decreased, while female affiliation towards the male increased. The increase of female tolerance and the changes in social behaviour were similar between the introductions, indicating a general pattern in female behaviour, although some variation in effect size and significance level was observed. Based on these results, we suggest that low female submission levels towards an introduced male may constitute a criterion to assess the risk of leaving the male in the group full-time. Moreover, low female aggression levels at the end of the introduction may signal long-term group stability. Overall, we conclude that female behaviour can provide valuable information about the male introduction process and should not be overlooked

Factors determining male introduction success and long-term stability in captive rhesus macaques

The entrance of new males into non-human primate groups bears high social risk, yet migration is necessary to prevent inbreeding. Males are not always accepted in their new group. In the wild, males may increase the likelihood of successful group entry by choosing a new group based on their own and the group's characteristics. Understanding whether these characteristics also determine a male's ability to enter captive groups is crucial to improve introduction management. This study aims to identify which factors determine male introduction success (i.e. male stays in the group for at least 4 weeks) and long-term stability (i.e. the male does not cause considerable behavioural problems after success) after male introductions in captive groups of rhesus macaques (Macaca mulatta), creating one-male groups. We studied 64 male introductions at the breeding colony of the Biomedical Primate Research Centre in Rijswijk, The Netherlands. 49 (77%) introductions were successful, with the male obtaining a long-term stable social position in the group in 38 (59%) introductions. Introductions of males that reached at least prime age, into groups with more adult females, but without pregnant females were most successful. Moreover, long-term stability was highest when males were heavier, were at least 3.5 years old when they were first removed from their natal group, and groups had few matrilines and no pregnant females were present. Males should be introduced at the time they would naturally immigrate, when they are strongest. Moreover, groups should consist of few large matrilines, as observed in the wild, with philoatric females and males that are removed at natural age. Our study highlights the importance of composing naturalistic groups and mimicking natural migration patterns to maintain long-term stable breeding groups in captivity

Factors determining male introduction success and long-term stability in captive rhesus macaques

The entrance of new males into non-human primate groups bears high social risk, yet migration is necessary to prevent inbreeding. Males are not always accepted in their new group. In the wild, males may increase the likelihood of successful group entry by choosing a new group based on their own and the group's characteristics. Understanding whether these characteristics also determine a male's ability to enter captive groups is crucial to improve introduction management. This study aims to identify which factors determine male introduction success (i.e. male stays in the group for at least 4 weeks) and long-term stability (i.e. the male does not cause considerable behavioural problems after success) after male introductions in captive groups of rhesus macaques (Macaca mulatta), creating one-male groups. We studied 64 male introductions at the breeding colony of the Biomedical Primate Research Centre in Rijswijk, The Netherlands. 49 (77%) introductions were successful, with the male obtaining a long-term stable social position in the group in 38 (59%) introductions. Introductions of males that reached at least prime age, into groups with more adult females, but without pregnant females were most successful. Moreover, long-term stability was highest when males were heavier, were at least 3.5 years old when they were first removed from their natal group, and groups had few matrilines and no pregnant females were present. Males should be introduced at the time they would naturally immigrate, when they are strongest. Moreover, groups should consist of few large matrilines, as observed in the wild, with philoatric females and males that are removed at natural age. Our study highlights the importance of composing naturalistic groups and mimicking natural migration patterns to maintain long-term stable breeding groups in captivity

A Stepwise Male Introduction Procedure to Prevent Inbreeding in Naturalistic Macaque Breeding Groups

Male introductions into captive primate breeding groups can be risky and unsuccessful. However, they are necessary to prevent inbreeding in naturalistic breeding groups. The procedure used to introduce new individuals may affect the success and influence the risks associated with group introductions. At the Biomedical Primate Research Centre (BPRC) in Rijswijk, the Netherlands, male rhesus macaque (Macaca mulatta) introductions into naturalistic social groups with a matrilineal structure and without a breeding male achieve relatively high success rates. This paper describes the male introduction procedure used at the BPRC. Males are stepwise familiarized with and introduced to their new group, while all interactions between the new male and the resident females are closely monitored. Monitoring the behaviour of the resident females and their new male during all stages of the introduction provides crucial information as to whether or not it is safe to proceed. The BPRC introduction procedure is widely applicable and may improve the management of captive primate groups in any housing facility worldwide. Thus, the careful introduction management can minimize the risk associated with male introductions and enhance the welfare of captive primates

A Stepwise Male Introduction Procedure to Prevent Inbreeding in Naturalistic Macaque Breeding Groups

Male introductions into captive primate breeding groups can be risky and unsuccessful. However, they are necessary to prevent inbreeding in naturalistic breeding groups. The procedure used to introduce new individuals may affect the success and influence the risks associated with group introductions. At the Biomedical Primate Research Centre (BPRC) in Rijswijk, the Nether-lands, male rhesus macaque (Macaca mulatta) introductions into naturalistic social groups with a matrilineal structure and without a breeding male achieve relatively high success rates. This paper describes the male introduction procedure used at the BPRC. Males are stepwise familiarized with and introduced to their new group, while all interactions between the new male and the resident females are closely monitored. Monitoring the behaviour of the resident females and their new male during all stages of the introduction provides crucial information as to whether or not it is safe to proceed. The BPRC introduction procedure is widely applicable and may improve the management of captive primate groups in any housing facility worldwide. Thus, the careful introduction management can minimize the risk associated with male introductions and enhance the welfare of captive primates