Abstract
Gibbons (family Hylobatidae) typically form groups that encompass a single breeding pair. Here, we present the first evidence of polygyny (where a single male has more than one female mate) in the Bornean white-bearded gibbon (Hylobates albibarbis). In July 2014, an adult female yet to have emigrated from her natal group gave birth to an infant, bringing the total group size to six individuals (one adult male, two adult females, one subadult female, and two infant females). Forty months later in November 2017, the same female gave birth to a second infant. Between July 2014 and April 2018, the two breeding females within the group remained mutually tolerant of each other, often singing the characteristic female vocalisation, the great call, in unison, until the eldest adult female dispersed in November 2018. We explore possible reasons behind this group’s mating system flexibility by examining dispersal limitation due to environmental constraints, factors associated with a large home range size, mutual tolerance between females, and a lack of mating opportunities.
Introduction
Primate social systems vary between species, within-species and even on a population level (Fleagle, 2013; Koenig et al., 2013). These variations are the result of specific ecological characteristics relating to access to resources (e.g., food and mates) and potential risks (e.g., predators) (Koenig et al., 2013). Different social systems are defined by looking at associated components, such as social structure (i.e., dispersal patterns and quality of relationships between conspecifics), social organisation (i.e., size, composition and cohesion), and mating system (i.e., how individuals mate and breed within their social system) (Dunbar, 1988; Kappeler and van Schaik, 2002; Kappeler, 2019). Four main mating systems have been identified in primate species: monogamy (exclusive mating relationship between one male and one female until disrupted, e.g., death, intruder, partner disperses etc.), polygyny (a single male has more than one female mate), polyandry (a single female has more than one male mate) and polygynandry (both males and females have multiple mates) (Strier, 2016; Huck et al., 2020). It is important to note that mating systems can be genetic (i.e., related to breeding, where an infant is conceived) or social (i.e., related to mating, which does not necessarily lead to conception). Terms associated with mating systems are often used inconsistently in the literature (Kappeler, 2019; Huck et al., 2020). For clarity, when discussing different “mating systems” in this paper, we are referring to mating and reproductive behaviour and not grouping patterns.
Gibbons (family Hylobatidae) are small arboreal apes found in east and southeast Asia. They typically live in small family units consisting of a single breeding pair and their offspring (O’Brien and Kinnaird, 2011). Both sexes of offspring usually emigrate from their natal group, often being pushed out by the same-sex parent once they have reached sexual maturity around eight years (Brockelman et al., 1998; Bartlett, 2011; Kappeler et al., 2013; Guan et al., 2013). Emigrating offspring move to a new home range to mate with a lone individual or displace a previously-mated individual in a “takeover” event (Mackinnon and Mackinnon, 1977; Brockelman et al., 1998). By dispersing, individuals avoid the risk of inbreeding (Wolff, 1993; Perrin and Mazalov, 2000), reduce local resource competition (Greenwood, 1980) and intra-group competition between same-sexed individuals (Dobson, 1982; Moore and Ali, 1984).
Monogamy is evident in only 14% of primates (Rutberg, 1983; Clutton-Brock, 2016) and can have associated benefits such as extra paternal investment (Borries et al., 2011). Early research suggested gibbons were strictly monogamous (Carpenter, 1940; Chivers, 1974; Srikosamatara, 1980). However, long-term studies have reported partner changes and extra-pair copulation events (EPCs) (a mating behaviour where an individual copulates furtively with a group outsider) (e.g., white-handed gibbon, Hylobates lar: Sommer and Reichard, 2000; Reichard, 2009), as well as polygynous mating systems (pileated gibbons, Hylobates pileatus: Srikosamatara and Brockelman, 1987; black crested gibbon, Nomascus concolor: Fan et al., 2006, Huang et al., 2013; Hainan gibbon, Nomascus hainanus: Liu et al, 1989; Zhou et al., 2005; 2008; Cao vit gibbon, Nomascus nasutus: Fan et al., 2010) and polyandrous mating systems (H. lar: Barelli et al., 2008; Reichard et al., 2012; siamang, Symphalangus syndactylus: Lappan, 2007; western hoolock, Hoolock hoolock: Siddiqi, 1986; Ahsan, 1995).
Observations of polygyny in gibbons were first published in 1987 (H. pileatus: Skrikosamatara and Brockelman, 1987). Of the four genera of gibbons, Nomascus species have the highest incidence of polygyny (Malone and Fuentes, 2009; N. nasutus: Fan et al. 2010; N. concolor: Fan and Jiang, 2009; N. hainanus: Zhou et al., 2005, 2008). Interestingly, some species of gibbon have flexibly adopted both monogamous and polygamous (i.e., polygyny or polyandry) mating systems, possibly as a response to external ecological and social factors (e.g., food and mate availability) (Kappeler et al., 2013; Sommer and Reichard, 2000). Polygyny has been hypothesised to be caused by either a lack of available habitat to disperse into upon reaching sexual maturity (Liu et al., 1989; Huang et al., 2013), larger home ranges requiring more individuals to defend (Rutberg, 1983; Jiang et al., 1999; Fan et al., 2015), and/or a mutual tolerance between sexually mature females within the same group (Srikosamatara and Brockelman, 1987; Liu et al., 1989; Jiang et al., 1999). Polygyny in many gibbon groups has been reported as being short-lived (i.e., lasting less than two years) (Fuentes, 1998; Fan et al., 2010). Gibbon groups exhibiting this mating system for longer have only been documented in Nomascus species (Zhou et al., 2005; Fan and Jiang, 2009; Fan et al., 2010).
This brief report presents the first evidence of polygyny recorded in Bornean white-bearded gibbons (Hylobates albibarbis). With current, long-term gibbon field studies running beyond 15 years, more reliable observations of group dynamics can now be made. Herein we give possible explanations for this rare occurrence observed in this species.
Materials and methods
Study location
These observations were documented by the Borneo Nature Foundation (BNF) in the Natural Laboratory of Peat Swamp Forest (NLPSF), Central Kalimantan, Indonesia (2°19′S and 113°54′E). The NLPSF is located 20 km southwest of the provincial capital, Palangka Raya, and is operated by the Centre for the International Cooperation in the Management of Tropical Peatlands (CIMTROP).
Study species
H. albibarbis is endemic to south-west Kalimantan between the Kapuas and Barito Rivers (Buckley et al., 2006). The species is found in primary and disturbed secondary tropical forest, as well as montane and lowland habitats, including peat-swamp forest (Nijman et al., 2008). H. albibarbis is currently listed as Endangered on the International Union for Conservation of Nature’s Red List of Threatened Species due to illegal trade, hunting and deforestation (Nijman et al., 2008; Cheyne et al., 2019). Previous research suggests this species displays a monogamous mating system (Gittins and Raemaekers, 1980; Cheyne and Chivers, 2006) with no records of polygamy to date. The average group size is 4.45 individuals (range: 3-5 individuals) (Cheyne et al., 2008; Cheyne, 2010). The inter-birth interval is 2.4 years and the gestation period lasts for ca. 210-270 days (7-9 months) (Cheyne, 2010).
Behaviour monitoring
Since 2005, BNF has been monitoring four habituated H. albibarbis groups with overlapping home ranges. More than 4449 h (1898 follow days on 44 individuals) have been collected (usually between 04:00 and 14:00). Of the groups studied, 2065 h (608 days) were spent observing group K between May 2005 and July 2019. The group was followed for up to eight days every month. We monitored group composition (including dispersal patterns, births and deaths) and copulation events, and recorded these observations ad libitum. Individuals were identified through detailed physical cues (e.g., eyebrows, beards, development of genitalia, body size) and behavioural criteria (e.g., singing, foraging dynamics, relative proximity to other group members). Individual identification guides (with photographs) were created to aid field researchers.
Results
Group K has been observed since 2005, enabling us to monitor life histories, changes in demographics, dispersal events, and the death and arrival of new infants. In 2005, group K consisted of an adult mated pair (a female called CL and a male called BL), the formation of which was before the study period, and two female offspring (ZZ and JL) (fig. 1). We estimated that ZZ was born in 2000 and dispersed from the group in 2011. JL was estimated to be born in 2003 and remained within her natal group despite being more than 10 years old. Between 2005 and 2012, CL gave birth to three other infants (KK, BRL and an unnamed infant). KK and the unnamed infant died of unknown causes in 2007 and 2012, respectively, whilst BRL dispersed from her natal group in 2016.
Family tree of group K. Males are represented by a rectangle, females by an oval. Offspring that dispersed or died during the study period are highlighted in grey. The dotted line indicates the unknown mate of JL.
Citation: Folia Primatologica 93, 1 (2022) ; 10.1163/14219980-20200801
In 2014, the adult females within group K, CL and JL, each gave birth to a female infant; CL to EL, and CRL to JL (figs 1 and 2). EL was CL’s fourth infant, born in April 2014. CRL was JL’s first infant, born in July 2014. There were numerous copulations recorded between CL and BL in the run-up to the births between December 2012 and January 2014 (fig. 2). An EPC involving CL was also recorded between an adult male (CA) in neighbouring group C in July 2013. No copulation attempts were observed between JL and any outside males. The arrival of the two infants, EL and CRL, increased the family group size to six individuals: one adult male, two adult females, one subadult female and two infant females (fig. 1). Between the births in 2014 and 2015, both adult females duetted with BL, singing their great calls in unison (fig. 2; see supplementary video S1).
Timeline of events for group K between December 2012 and November 2018, highlighting copulations, shared singing behaviour and births.
Citation: Folia Primatologica 93, 1 (2022) ; 10.1163/14219980-20200801
In May 2016, a copulation was observed between JL and BL. In November 2017, JL gave birth to her second infant female, JNL (figs 1 and 2). Between 2016 and 2017, CL appeared to travel further away from the rest of her group, but still joined the duet and great call with BL and JL. In September 2018, there was an aggressive encounter between BL and CL, when he attacked her. The context was unknown. No aggressive or displacement behaviours have ever been recorded between CL and JL. On 25 November 2018, CL was observed travelling farther away from the group before being chased away by her own group. CL then disappeared and was not observed up until July 2019. Based on anecdotal evidence since this publication, we believe that CL was forced out of the group permanently while her youngest offspring, EL, remained.
Discussion/conclusion
Monogamy was thought to occur in about 14 to 15% of primates (Rutberg, 1983; Clutton-Brock, 2016), but our definition of monogamy has more recently been subject to reassessment, owing to more detailed observations and the availability of genetic information. With numerous observations of partner changes and EPCs occurring in many “monogamous” mammals (Hughes, 1998) including gibbons (Palombit, 1994; Reichard, 1995; Barelli et al., 2013), the traditional definition of “monogamy” has since been challenged (Tecot et al., 2016). As evident in this study, an EPC involving the adult female, CL, was observed during an intergroup encounter. Although no EPCs were recorded for JL, it is possible that these events occurred but were not recorded due to the difficulty of identifying individuals during brief intergroup encounters, or occurred on non-follow days.
In the genus of Hylobates, cases of polygyny are rare (Malone and Fuentes, 2009) and have been short-lived (i.e., lasting less than two years) (Fuentes, 1998; Sommer and Reichard, 2000). Even Nomascus species which demonstrate a higher incidence of polygyny (Zhou et al., 2005; Fan and Jiang, 2009; Fan et al., 2010), have cases of mature subadult gibbons eventually replacing the adult male or female in their natal groups (N. concolor: Huang et al., 2013). Although we recorded no aggressive encounters between CL and JL, the departure of CL in November 2018 resulted in JL eventually replacing her mother. Our long-term observational study of a H. albibarbis group verifies that they exhibited a polygynous mating system for approximately four years, making it the longest observation in Hylobates. Reasons for its occurrence are not fully understood, but we explore several possible explanations below: (1) lack of optimal quality habitat to disperse to; (2) mutual tolerance between females and/or shortage of mating opportunities; and (3) home range size indicators.
Lack of optimal quality habitat
Polygyny in gibbons has previously believed to have occurred in response to a lack of optimal quality habitat for individuals to disperse to and find mates (Liu et al., 1989; Huang et al., 2013). Group K resided in a degraded peat-swamp forest which, although protected since 2004, has faced many years of disturbance from illegal logging and forest fires (Harrison et al., 2007; Cheyne et al., 2019). Furthermore, the peat-swamp forest is recognised as a low-productivity habitat (Morrogh-Bernard et al., 2003) with important seasonal fluctuations of fruit availability (Cheyne, 2010; Harrison et al., 2016). In 2015, forest fires devastated 53.8 km2 of habitat in NLPSF (Cheyne et al., 2019). Although this forest loss has reduced available gibbon habitat in the region, group K’s home range did not appear to be directly impacted. In fact, group K maintained a large home range of 154 ha (Cheyne et al., 2019). Although the peat-swamp forest is considered to be a low-productivity habitat, food is available year round (Harrison et al., 2010). We, therefore, discount a lack of available habitat as a possible enabler for the observed polygyny.
Mutual tolerance and mating opportunities
Although not necessarily a driver of polygyny, mutual tolerance between breeding female gibbons would support it, and also benefit group cohesion when defending food resources and reducing predation risk. Nevertheless, subadult female gibbons approaching sexual maturity would not normally be tolerated by the adult female within the same group (Jiang et al., 1999). During a 20-month study on N. concolor, no displacement or aggressive encounters were recorded between two adult females however, suggesting that mutual tolerance allowed more than one breeding female to reside in the group (Jiang et al., 1999). Similar observations have been recorded in N. hainanus (Liu et al., 1989) where the females fed amicably, and in H. pileatus where the great call was sung in unison (Srikosamatara and Brockelman, 1987). No bouts of aggression or displacement were observed between JL and CL, and they were recorded regularly singing the great call together, often in proximity with BL, thus suggesting a mutual tolerance between the adult females.
Mutual tolerance alone does not explain polygyny, however. Although dispersal patterns of gibbons in NLPSF are still poorly understood, there does appear to be a limited number of available breeding males in the region (for reasons unknown). Furthermore, other groups that are followed regularly have subadult males who are more than 12 years of age and yet to emigrate from their natal group, indicating a delayed dispersal.
Home range size indicators
Generally, home ranges across gibbon species vary between 7 and 58 ha (Leighton, 1987). Gibbon groups exhibiting polygynous mating systems have been known to occupy up to 500 ha however, demonstrating a possible relationship between mating system, group size and habitat area (N. hainanus: Liu et al., 1989). Larger home ranges have the resources to sustain two or more breeding females and their offspring (Jiang et al., 1999; Fan et al., 2015). Females have been speculated to benefit from these larger home ranges by having greater access to resources, therefore improving their overall chances of reproductive success and fitness (Guan et al., 2017).
Drivers behind group K’s large home range size could be due to a lack of intergroup competition in the NLPSF, and/or the “Resource Dispersion Hypothesis” (where resources are patchily distributed across a large area so a group of animals will share the same space with little to no feeding competition) (Macdonald, 1983; Kruuk and Macdonald, 1985; Carr and Macdonald, 1986). Whilst some groups in NLPSF are limited by their home range abutting the forest edge and therefore are unable to expand, group K have few neighbours to the west (possibly due to a population decline in the early 2000’s associated with logging in the region) (Cheyne, pers. obs.). The “Resource Dispersion Hypothesis” can be discounted in the NLPSF, however, as food is available throughout the year (Harrison et al., 2010) and the gibbons have little variation in their home range use (Singh et al., 2018; Cheyne et al., 2019).
In summary, we suggest that a lack of neighbouring groups and competition for food and space could have facilitated group K’s large home range size. This, coupled with delayed male dispersal and a female skew in the population, as well as intragroup female tolerance, could have enabled the polygyny observed in group K. Genetic testing would confirm paternity of all offspring and help to explain some of the intragroup relationships. It would also improve our knowledge of gibbon dispersal patterns, an area of research that is still understudied.
In this brief report, we have not only highlighted the first recorded observation of polygyny in this species, but also the value of long-term monitoring to improve our understanding of gibbon mating systems. The implications of a polygynous mating system in this region (e.g., inbreeding and overcrowding) are unknown and therefore there is huge benefit in continued long-term monitoring. Furthermore, with anthropogenic activities and habitat loss increasing in this region, we may see more intergroup interactions and conflicts, EPCs, and less available optimal habitat for the formation of new gibbon groups, thus impacting mating systems with unknown consequences.
Corresponding author; e-mail: carolyn.thompson.17@ucl.ac.uk
Acknowledgements
We wish to thank RISTEK for supporting this research, as well as our partners, CIMTROP, and all the BNF staff, volunteers, students and interns who have worked on the gibbon project since 2005. We also thank Axel Martinez Ruiz and Jenny Grib for their technical knowhow. Finally, we wish to thank the reviewers for their constructive comments and for strengthening our manuscript.
Statement of ethics
This field study has no ethical conflicts to disclose. The research was approved locally by RISTEK (HB: 225/SIP/FRP/SM/VI/2013, CT: 043/SIP/FRP/SM/II/2014 and SMC: 217-A/SIP/FRP/SM/I/2014) and complies with the Association for the Study of Animal Behaviour guidelines for the treatment of animals in behavioural research.
Conflict of interest statement
The authors have no conflicts of interest to declare.
Funding sources
Arcus Foundation; US Fish and Wildlife Great Ape Fund.
Author contributions
All authors assisted with data collection in Indonesia under SMC’s project management and CT’s field supervision. As first and corresponding author, CT led on the writing of the manuscript. EC, HB and SMC contributed to the writing and editing of the manuscript. AK and EC prepared the data. CT, HB and SMC prepared the figures. All authors edited the final manuscript.
Supplementary material
Supplementary material is available online at: https://doi.org/10.6084/m9.figshare.18709058
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