Male-infant interactions in wild crested black macaques, Macaca nigra

Direct fitness is measured as the number of surviving offspring. Thus adult males may try to produce as many offspring as possible or to increase the survival of their offspring. Recent findings have shown the many potential benefits of fathers’ presence and support on infants’ development and survival. However, little is known about the influence of socio-ecological factors on male-infant interactions. The main aim of this thesis was therefore to investigate male-infant interactions in wild crested macaques (Macaca nigra). In particular, we aimed to examine the affiliative and agonistic interactions taking place in this species, along with the factors influencing these interactions and offspring survival. Data collection for this thesis took place in the Tangkoko-Duasudara Reserve in Sulawesi, Indonesia, on 3 wild groups of crested macaques. For the first study, data were collected on migrations, births, disappearances, and encounters between groups over 5 years. We analyzed the influence of socio-ecological factors (e.g. rainfall, alpha-male position takeover, and male hierarchy stability) on pre- and post-natal loss. The results showed that high infant mortality was mainly associated to male alpha-position takeover, which suggests that infanticide may indeed occur in this species. In addition, we found that female within-group competition for food sources and between-group resource defense influenced fetal and infant loss. Based on these findings, we were interested to see whether fathers protected their own offspring against male attacks. Thus, in the second study, we investigated the social determinants and characteristics of male-infant affiliations. Our results indicate that adult males and infants form preferential association, and that infants initiate the majority of male-infant affiliations. Infants initiated affiliations mainly towards a high ranking male or a male in a close relationship with their mother. In addition, infants affiliated mainly with adult males in the absence of their mother, while males affiliated mostly with infants when the infants‘ mother was present in proximity. Furthermore, males initiated affiliations towards an infant when they held a high rank or when they had a strong bond with the infant‘s mother. Interestingly, paternity did not affect male-infant affiliations. In conclusion, these studies provide insights in the specifics of both infant survival strategies and male reproductive strategies. In addition, we show that infants are active agents in establishing and maintaining preferential relationships with males. This thesis, thus, confirm that male-infant interactions, although rare, have a strong influence both on males’ and infants’ direct fitness.:Contents ........................................................................................................................................ 5 List of Figures .............................................................................................................................. 7 List of Tables ................................................................................................................................ 8 Summary ....................................................................................................................................... 9 Zusammenfassung .................................................................................................................. 13 1 General Introduction .......................................................................................................... 17 1.1 Infants and adult males in mammals ...................................................................... 18 1.2 Primate males’ use and abuse of infants ................................................................ 19 1.3 Male care and paternal care in primates ............................................................... 20 1.4 Crested macaques as study species ......................................................................... 21 1.5 Aims of this thesis ........................................................................................................... 23 2 Social and ecological factors influencing offspring survival in wild macaques ................................................................................................................................... 25 2.1 Abstract ............................................................................................................................... 26 2.2 Introduction ...................................................................................................................... 26 2.3 Methods .............................................................................................................................. 29 2.4 Results ................................................................................................................................. 34 2.5 Discussion .......................................................................................................................... 37 3 Mother-male bond, but not paternity, influences male-infant affiliation in wild crested macaques .......................................................................................................... 45 3.1 Abstract ............................................................................................................................... 46 3.2 Introduction ...................................................................................................................... 46 3.3 Methods .............................................................................................................................. 50 3.4 Results ................................................................................................................................. 58 3.5 Discussion .......................................................................................................................... 61 4 Thesis Conclusion ................................................................................................................ 71 Appendices ................................................................................................................................ 75 Supplementary figure and tables for Chapter 2 ......................................................... 76 Supplementary methods and tables for Chapter 3 ................................................... 79 Bibliography ............................................................................................................................. 83 Acknowledgements ................................................................................................................ 99 Contributions of co-authors .............................................................................................. 101 Curriculum vitae .................................................................................................................... 105 Publications and conference contributions ................................................................. 107 Selbstständigkeitserklärung ............................................................................................. 10

Mother-male bond, but not paternity, influences male-infant affiliation in wild crested macaques

In promiscuous primates, interactions between adult males and infants have rarely been investigated. However, recent evidence suggests that male affiliation towards infants has an influence on several aspects of the infants’ life. Furthermore, affiliations may be associated with male reproductive strategy. In this study, we examined which social factors influenced male-infant affiliation initiated by either male or infant, in wild crested macaques (Macaca nigra). We combined behavioral data and genetic paternity analysis from 30 infants living in three wild groups in Tangkoko Reserve, Indonesia. Our results indicate that adult males and infants do not interact at random, but rather form preferential associations. The social factors with the highest influence on infant-initiated interactions were male rank and male association with the infant’s mother. While infants initiated affiliations with males more often in the absence of their mothers, adult males initiated more affiliations with infants when their mothers were present. Furthermore, males initiated affiliations more often when they were in the same group at the time the infant was conceived, when they held a high dominance rank or when they had a close relationship with the mother. Interestingly, paternity did not affect male-infant affiliation despite being highly skewed in this species. Overall, our results suggest that adult males potentially associate with an infant to secure future mating with the mother. Infants are more likely to associate with a male to receive better support, suggesting a strategy to increase the chance of infant survival in a primate society with high infant mortality

Social and ecological factors influencing offspring survival in wild macaques.

Premature loss of offspring decreases direct fitness of parents. In gregarious mammals, both ecological and social variables impact offspring survival and may interact with each other in this regard. Although a number of studies have investigated factors influencing offspring loss in mammals, we still know very little on how different factors interact with one another. We therefore investigated fetal and infant mortality in 3 large groups of wild crested macaques (Macaca nigra) over a period of up to 5 years by including potential social causes such as maternal dominance rank, male immigration, between group encounters, and ecological conditions such as rainfall in a multivariate survival analysis using Cox proportional hazards model. Infant but not fetal survival was most impaired after a recent takeover of the alpha-male position by an immigrant male. Furthermore, infant survival probability increased when there was an increase in number of group adult females and rainfall. Fetal survival probability also increased with an increase of these 2 factors, but more in high-ranking than low-ranking females. Fetal survival, unlike that of infants, was also improved by an increase of intergroup encounter rates. Our study thus stresses the importance of survival analyses using a multivariate approach and encompassing more than a single offspring stage to investigate the determinants of female direct fitness. We further provide evidence for fitness costs and benefits of group living, possibly deriving from high pressures of both within- and between-group competition, in a wild primate population

Training future generations to deliver evidence-based conservation and ecosystem management

1. To be effective, the next generation of conservation practitioners and managers need to be critical thinkers with a deep understanding of how to make evidence-based decisions and of the value of evidence synthesis. 2. If, as educators, we do not make these priorities a core part of what we teach, we are failing to prepare our students to make an effective contribution to conservation practice. 3. To help overcome this problem we have created open access online teaching materials in multiple languages that are stored in Applied Ecology Resources. So far, 117 educators from 23 countries have acknowledged the importance of this and are already teaching or about to teach skills in appraising or using evidence in conservation decision-making. This includes 145 undergraduate, postgraduate or professional development courses. 4. We call for wider teaching of the tools and skills that facilitate evidence-based conservation and also suggest that providing online teaching materials in multiple languages could be beneficial for improving global understanding of other subject areas.Peer reviewe

Male-infant interactions in wild crested black macaques, Macaca nigra

Direct fitness is measured as the number of surviving offspring. Thus adult males may try to produce as many offspring as possible or to increase the survival of their offspring. Recent findings have shown the many potential benefits of fathers’ presence and support on infants’ development and survival. However, little is known about the influence of socio-ecological factors on male-infant interactions. The main aim of this thesis was therefore to investigate male-infant interactions in wild crested macaques (Macaca nigra). In particular, we aimed to examine the affiliative and agonistic interactions taking place in this species, along with the factors influencing these interactions and offspring survival. Data collection for this thesis took place in the Tangkoko-Duasudara Reserve in Sulawesi, Indonesia, on 3 wild groups of crested macaques. For the first study, data were collected on migrations, births, disappearances, and encounters between groups over 5 years. We analyzed the influence of socio-ecological factors (e.g. rainfall, alpha-male position takeover, and male hierarchy stability) on pre- and post-natal loss. The results showed that high infant mortality was mainly associated to male alpha-position takeover, which suggests that infanticide may indeed occur in this species. In addition, we found that female within-group competition for food sources and between-group resource defense influenced fetal and infant loss. Based on these findings, we were interested to see whether fathers protected their own offspring against male attacks. Thus, in the second study, we investigated the social determinants and characteristics of male-infant affiliations. Our results indicate that adult males and infants form preferential association, and that infants initiate the majority of male-infant affiliations. Infants initiated affiliations mainly towards a high ranking male or a male in a close relationship with their mother. In addition, infants affiliated mainly with adult males in the absence of their mother, while males affiliated mostly with infants when the infants‘ mother was present in proximity. Furthermore, males initiated affiliations towards an infant when they held a high rank or when they had a strong bond with the infant‘s mother. Interestingly, paternity did not affect male-infant affiliations. In conclusion, these studies provide insights in the specifics of both infant survival strategies and male reproductive strategies. In addition, we show that infants are active agents in establishing and maintaining preferential relationships with males. This thesis, thus, confirm that male-infant interactions, although rare, have a strong influence both on males’ and infants’ direct fitness.:Contents ........................................................................................................................................ 5 List of Figures .............................................................................................................................. 7 List of Tables ................................................................................................................................ 8 Summary ....................................................................................................................................... 9 Zusammenfassung .................................................................................................................. 13 1 General Introduction .......................................................................................................... 17 1.1 Infants and adult males in mammals ...................................................................... 18 1.2 Primate males’ use and abuse of infants ................................................................ 19 1.3 Male care and paternal care in primates ............................................................... 20 1.4 Crested macaques as study species ......................................................................... 21 1.5 Aims of this thesis ........................................................................................................... 23 2 Social and ecological factors influencing offspring survival in wild macaques ................................................................................................................................... 25 2.1 Abstract ............................................................................................................................... 26 2.2 Introduction ...................................................................................................................... 26 2.3 Methods .............................................................................................................................. 29 2.4 Results ................................................................................................................................. 34 2.5 Discussion .......................................................................................................................... 37 3 Mother-male bond, but not paternity, influences male-infant affiliation in wild crested macaques .......................................................................................................... 45 3.1 Abstract ............................................................................................................................... 46 3.2 Introduction ...................................................................................................................... 46 3.3 Methods .............................................................................................................................. 50 3.4 Results ................................................................................................................................. 58 3.5 Discussion .......................................................................................................................... 61 4 Thesis Conclusion ................................................................................................................ 71 Appendices ................................................................................................................................ 75 Supplementary figure and tables for Chapter 2 ......................................................... 76 Supplementary methods and tables for Chapter 3 ................................................... 79 Bibliography ............................................................................................................................. 83 Acknowledgements ................................................................................................................ 99 Contributions of co-authors .............................................................................................. 101 Curriculum vitae .................................................................................................................... 105 Publications and conference contributions ................................................................. 107 Selbstständigkeitserklärung ............................................................................................. 10

The current status of the world’s primates: Mapping threats to understand priorities for primate conservation

Over the past decades, primate populations have been declining. Four years ago, >60% of species were listed as threatened. As the rate of loss accelerates and new IUCN assessments are being published, we used IUCN Red List assessments and peer-reviewed literature published within the last 5 yr to evaluate the status of primates globally, by region and by taxonomic group. We also examined the main factors affecting a species’ conservation status to determine if we could predict the status of understudied species. We found that 65% of species are in the top three IUCN Red List categories (Vulnerable, Endangered, Critically Endangered). Globally, the main threats to primates are Biological Resource Use, including Hunting & Logging, and Agriculture. The impact of these threats varied by region and taxon. Our model showed that Malagasy and Asian primates, and those affected by Agriculture, Human Disturbance, and Climate Change were more likely to be considered at risk of extinction. The model’s predictive probability, however, was low. Our literature analysis showed that some threats, especially climate change and disease, affected more species than indicated by the IUCN Red List. As we move into the next decade, we must continue tackling hunting and agricultural expansion but also be vigilant about emerging threats. We must also aim to regularly test the effectiveness of mitigation strategies, evaluating their long-term adoption and their impact on primates; as well as to increase communication between researchers and applied conservationists to ensure IUCN assessments include current and emerging threats