Kingdom Animalia Phylum Chordata
Class Mammalia Order Primates Suborder Haplorrhini
Parvorder Catarrhini Superfamily Cercopithecoidea
Family Cercopithecidae Subfamily Cercopithecinae
Tribe Papionini Genus Macaca Species Macaca assamensis
Figure 1.1: An adult male Assamese macaque in Phu Khieo Wildlife Sanctuary, Thailand. Picture by Daria R. Gutleb.
1.5.1 General background
Macaques (Macaca spp.) are monophyletic and diverged from a common ancestor with humans approximately 25 - 28 million years ago (Kumar & Hedges, 1998; Morales
& Melnick, 1998; Rogers & Gibbs, 2014). The genus name Macaca derives from the word “ma-kako”, meaning “monkey” in a Congolese Bantu language (‘macaca’, 2000).
Except for humans, macaques have the largest geographic range among primates and are among the best-studied taxa (Thierry et al., 2004). Paleontological findings from the Pleistocene show that macaques existed from North Africa, through Europe to Asia (Abegg & Thierry, 2002; Delson, 1980; Eudey, 1980; Fa, 1989). Today, only one relict species inhabits Northern Africa, the Barbary macaque (Macaca sylvanus), and the other 22 known macaque species all occur only in Asia. The present macaques can be divided into seven species groups: sylvanus, silenus, Sulawesi macaques, sinica, fascicularis, mulatta and arctoides (Zinner et al., 2013).
The study species in this thesis is the Assamese macaque (Macaca assamensis MCCLELLAND 1839, Figure 1.1) which is a member of the sinica group of macaques, next to Macaca sinica, radiata and thibetana (Fooden, 1980; Zinner et al., 2013). Assamese macaques can be divided into two sub-species, the Eastern (or Southeast Asian) Assamese macaque (Macaca assamensis assamensis) and the Western (or sub-Himalayan) Assamese macaque (Macaca assamensis pelops HODGSON 1840). With a currently decreasing population trend, both sub-species are classified as near threatened according to The IUCN Red List of Threatened Species (The IUCN Red List of Threatened Species, 2017). Habitat degradation and poachers constitute the main threat (The IUCN Red List of Threatened Species, 2017).
The population that was investigated in this thesis belongs to the Eastern Assamese macaque, which occurs between 200 and 2750 m above sea level in China, Tibet, India, Myanmar, Thailand, Laos and Vietnam (Brandon-Jones et al., 2004; Eudey, 2013; Fooden, 1982). This brownish colored macaque has habitats in subtropical and tropical, evergreen and semi-evergreen, deciduous and mixed bamboo, wet and dry, lowland and mountainous forests (Eudey, 2013). Assamese macaques are sexually dimorphic, with males being larger (head-body 53 - 73 cm) and heavier (8 - 17 kg) than
females (17 - 29 cm, 5 - 9 kg, Eudey, 2013; Fooden, 1982). They are mainly vegetarian, but the diet also includes insects and small vertebrates such as lizards and squirrels (Eudey, 2013; Koirala et al., 2017; Mitra, 2002; Schülke et al., 2011; Zhou et al., 2011).
Like in many macaque species, there exist groups that are provisioned, raid crops or beg for food from tourists (Aggimarangsee, 1992; Chalise, 2003; Eudey, 2013; Fooden, 1982;
Kaewpanus et al., 2015; Sarkar, 2014b). In captivity this primate can reach the age of approximately 28 years (Dathe, 1983; Eudey, 2013).
In the following section, I will describe those features of Assamese macaques which appear relevant for the studies that I conducted in this thesis: their dominance hierarchy, social behavior and seasonality. Afterwards, I will introduce the population of Assamese macaques that has been studied for this thesis: four wild groups living in their natural habitat in Phu Khieo Wildlife Sanctuary (PKWS) in Thailand.
1.5.2 Hierarchy, sociality and seasonality
Like all macaque species, Assamese macaques live in multimale-multifemale groups with males being the dispersing sex (Thierry et al., 2004). Females usually stay within their natal group lifelong, therefore matrilineal kin plays a particularly important role in female social relationships (Thierry et al., 2004).
Macaques can be classified into four grades according to the strictness of the female dominance hierarchy, aggression and conflict management (Thierry, 2000;
Thierry et al., 2008). Nepotism and the asymmetry of agonistic outcomes decline, whereas reconciliatory behavior increases from grade 1 to 4. Assamese macaques are classified as grade 2 macaques with a strict linear steep dominance hierarchy (Bernstein
& Cooper, 1999; Cooper & Bernstein, 2008; Macdonald et al., 2013; Ostner et al., 2008a, 2011). Female macaques acquire ranks close to their mothers, which is referred to as a
“classical nepotistic hierarchy” or a “classical matrilineal dominance structure” (Chapais, 2004). Therefore, a female’s rank position is quite stable and predictable from knowledge on her kinship. Males disperse at the age of puberty, but can continue to migrate between groups later in life (van Noordwijk & van Schaik, 2004; Thierry, 2007). Also, they can
change their dominance rank position throughout their life (Schülke et al., 2010). To acquire a higher rank, male-male coalitions are of particular importance (Schülke et al., 2010). Males who have strong social bonds form coalitions, which in turn predict future dominance and reproductive success (Schülke et al., 2010).
Assamese macaques may allocate up to almost a quarter (10 - 24 %) of their daily time for social activities, depending on food availability (Chalise, 1999; Koirala et al., 2017; Pandey & Chalise, 2015; Paudel & Chalise, 2017; Sarkar et al., 2012; Sarkar, 2014b, 2014a). Female Assamese macaques groom other females and juveniles more often than males do (Cooper & Bernstein, 2000), and reconcile more often with strong grooming partners (Cooper et al., 2005). Importantly, male Assamese macaques form strong and stable social bonds with females (Haunhorst et al., 2016; Ostner et al., 2013), but also males (Kalbitz et al., 2016, 2017). In primates, social bonds among males are generally rare and male Assamese macaques stand out in this regard (Ostner & Schülke, 2014).
Assamese macaques are seasonal breeders with a distinct birth/non-mating season from March to September and a mating season from October to February (Fooden, 1971;
Fürtbauer et al., 2010; Mitra & Alfred, 2007). The mating season is characterized by distinct behavioral and physiological changes. Males show increased levels of aggression, GCs and androgens (Ostner et al., 2008a, 2011). During the winter months, females have concealed ovulations, synchronize mating, show distinct promiscuity and initiate 70 % of all copulations (Fürtbauer et al., 2010, 2011a, 2011b). Females gestate 5.5 months and give birth every 1 to 2 years (Fürtbauer et al., 2010). Due to the behavioral and hormonal changes between the non-mating and the mating period, any study investigating long-term data must take the season when data were collected into account.
1.5.3 Assamese macaques in Phu Khieo Wildlife Sanctuary
The study population in PKWS ranges in the area of Huai Mai Sot Yai (16°5’-35’N, 101°20’-55’E, 600 - 800 m above sea level) in the province of Chaiyaphum in Isan, the north-eastern part of Thailand. With an 1543 km2 area of predominantly undisturbed dry evergreen and hill evergreen forest with bamboo patches, PKWS is a major part of the 6500 km2 protected Western Isaan Forest Complex (Borries et al., 2002; Grassman et al., 2005). The research field site in PKWS was established by A. König and C. Borries, who firstly described the diurnal primate community in PKWS (Borries et al., 2002) and studied the socio-ecology of Phayre's leaf monkeys (Trachypithecus phayrei, Borries et al., 2004; Koenig et al., 2004a, 2004b). Besides Assamese macaques, the sanctuary harbors the following seven primate species: white-handed gibbons (Hylobates lar), Phayre’s and silvered leaf monkeys (Trachypithecus cristatus), slow loris (Nycticebus coucang), stump-tailed (Macaca arctoides), pig-tailed (Macaca nemestrina) and rhesus macaques (Borries et al., 2002).
Since 2005 research on the study population of wild Assamese macaques in their natural habitat in PKWS is directed by J. Ostner and O. Schülke. It began with the effort to habituate first one, then two groups of Assamese macaques (AS and AO). The groups split in 2012 and 2014, respectively, thus four groups have been observed since then (ASM, ASS, AOM and AOS). Due to natural and frequent male migrations, groups experience a natural genetic flow (in contrast to laboratory or semi-free groups of primates). Also, one rare case of an immigrated female was observed. Only the researchers within the long-term project and occasionally rangers have access to the study groups, tourists are not allowed to enter the forest. Students continuously collect data following standardized observation and sampling protocols to assure the usability of data for long-term analysis. They do not interact with or feed the monkeys and try to keep a minimum distance of 5 m to observe natural behavior without disturbance.
As partially described above, the study population exhibits a strong seasonality in reproduction (Fürtbauer et al., 2010, 2013) and males react to the challenges of the mating season with a pronounced increase in aggression rates and GC output (Ostner et al. 2008a, 2011). Males can be ordered along a linear, relatively steep dominance
hierarchy (Ostner et al. 2008a) and individual paternity success increases with increasing dominance rank (Schülke et al. 2010; Sukmak et al. 2014a). Further, previous studies on the wild Assamese macaques in PKWS included research on their ecology (Schülke et al., 2011), females’ mating synchrony and concealed fertility (Fürtbauer et al., 2011a, 2011b), feeding competition (Heesen et al., 2013, 2014, 2015), immature development (Berghänel et al., 2015, 2016), molecular analyses of mitochondrial DNA, microsatellites and adenoviruses from non-invasively collected fecal samples (Müller et al., 2014; Sukmak et al., 2014b, 2017), male-male, male-female and male-infant relationships (Haunhorst et al., 2016, 2017, Kalbitz et al., 2016, 2017; Minge et al., 2016; Ostner et al., 2013; Ostner
& Schülke, 2018) and other aspects of their sociality (Macdonald et al., 2013; Richter et al., 2016; Schülke et al., 2010, 2014).
Regarding this range of research topics, the behavioral genetics approach in this thesis is new not only regarding the lack of genetic studies on wild primate behavior, but also a new approach in the long-term field project in PKWS. Considering that individual variation in GC levels and aggression as well as the causal connection between male social bonds and reproductive success have been previously demonstrated in this population of Assamese macaques (Ostner et al., 2008a; Schülke et al., 2010), they serve as ideal study animals to investigate the genetic underpinnings of behavior and hormones associated with the primate HPA-axis. Due to research on wild primates living in a protected area, all studies on the Assamese macaques of PKWS are of completely non-invasive nature. For my studies, I therefore collected fecal samples for non-non-invasive genetic analyses and urine samples for non-invasive hormone analyses from all four currently observed groups.