Social affiliation among sub-adult male koalas in a high-density population
Darcy J. Watchorn A B *A
B
Abstract
Koalas are generally considered to be a solitary species. However, during observations of free-ranging koalas in a high-density population, sub-adult males (3.5–5.5 years) were seen engaging in affiliative behaviours, including grooming, genital sniffing, and vocalising. These interactions were exclusive to males of this age group and are likely a result of the unusually high population density. In such populations, where home range overlap is common, these behaviours may help reduce stress, establish dominance hierarchies, and reduce conflict through familiarisation.
Keywords: animal behaviour, Koala, marsupial, Otway Ranges, Phascolarctos cinereus, population density.
Introduction
Most animals exhibit some form of social behaviour, typically related to courtship, reproduction, parental care, aggression, or social affiliation (Fischer et al. 2019). Social affiliation behaviours – such as grooming, maintaining physical proximity, cooperative activities, and vocalisations – are particularly prevalent among highly social, group-living species (Beery et al. 2009; Soriano Jimenez et al. 2021; Davila-Ross and Palagi 2022; Brooks and Burghardt 2023). These behaviours play a crucial role in forming and maintaining social bonds within a group (Fischer et al. 2019). In contrast, social interactions among solitary animals are infrequent and often limited to brief courtship encounters or territorial disputes (Kleiman and Eisenberg 1973; Sandell 1989). Consequently, solitary species are less likely to develop complex or adaptive social behaviours (Dammhahn and Kappeler 2009).
The koala (Phascolarctos cinereus) is generally regarded as a solitary species with a spatial organisation facilitated by long-distance vocalisations (Martin and Handasyde 1999; Charlton et al. 2013, 2017; Ellis et al. 2015; Jiang et al. 2022). However, koalas can engage in regular physical interactions during the breeding period (Ellis et al. 2015; Watchorn and Whisson 2019). In high-density populations, these interactions typically take the form of aggressive territorial encounters between males, aggressive copulation attempts between males and females, or – less frequently – interactions between males and joeys during copulation attempts (Melzer et al. 2010; Watchorn and Whisson 2019, 2023).
As expected for a largely solitary species, reports of social affiliation behaviours among adult or sub-adult koalas – such as grooming and non-aggressive physical proximity – are exceedingly uncommon. However, one study from a high-density population on French Island reported observations of sub-adult male koalas engaging in such behaviour (Mitchell 1990a, 1990b). Whilst the specific behaviours were not described in detail, Mitchell (1990a) suggested that ‘…young males seemed to seek the company of other young males…’, and that there is an absence of aggression in these interactions. There are no other published observations of this behaviour.
This paper presents previously unreported observations of social affiliation behaviours in free-ranging sub-adult koalas. These observations were made during the fieldwork for a previously published study on koala interactions in a high-density population in southeastern Australia (Watchorn and Whisson 2019). I then discuss the potential evolutionary function of such behaviours.
Methods
Study area and animal capture
The study was undertaken during the koala breeding season (Whisson et al. 2016) from August to December 2015 at Cape Otway, Victoria, Australia (38.8500°S, 143.5167°E). At the time of the study, the mean annual rainfall was 898 mm and the mean maximum temperature was 17oC (BoM 2015). The study area comprised fragmented manna gum (Eucalyptus viminalis) woodland, coastal heathland, and cleared pasture. The koala population density in the site was exceedingly high at the time of this study (up to 15 koalas/ha; Watchorn and Whisson 2019) following the release of koalas to the area in 1981 and subsequent rapid population growth (Whisson et al. 2016; Watchorn and Whisson 2019).
Koalas with a tooth-wear class (TWC) ranging from 3 to 7 (3.5–14+ years) were classified as sexually mature (McLean 2003; Whisson and Carlyon 2010). All 16 sexually mature males within the site were captured and fitted with VHF and proximity logger collars during August and early September (Watchorn and Whisson 2019). Additionally, five younger males at the site (TWC 2, 1.25–3.5 years) were tagged with uniquely numbered ear tags. A comprehensive survey of the site on 22 September suggested that all resident males in the site had been captured and processed at that time (Watchorn and Whisson 2019). Relatedness between individual koalas was unknown.
Interactions
Each collared male was tracked and observed for a minimum period of 30 min for five consecutive nights in September and October, and 11 nights in November (up to 17 nights per male). Observations were conducted between 21:00 and 2:00 hours, corresponding to the period of peak activity of koalas in the area (Ryan et al. 2013). When a male–male interaction was observed, the observation period was extended to encompass the interaction to its completion, the longest of which lasted 2 h (Watchorn and Whisson 2019). Behaviours associated with interactions were coded as either sexual, passive, or agonistic, and their time and duration were recorded (Watchorn and Whisson 2019).
Results and discussion
Seven male–male interactions were observed; six during the peak activity period (21:00–02:00 hours) and one during the day (12:25–13:05 hours). Of these, five interactions were agonistic and of short duration (median: 3 min 49 s; Watchorn and Whisson 2019). However, two interactions were passive and lengthy in nature (40 min and 2 h, respectively). These interactions involved three sub-adult males between 3.5 and 5.5 years of age: M06 (7.52 kg), M16 (7.71 kg), and M11 (6.94 kg). I describe these two interactions below.
Interaction one
This interaction involved all three sub-adult males (M06, M11, M16) and occurred over at least 2 h. The three males were first observed sitting within 1–2 m of one another on a large lateral branch (Fig. 1a). Initially, two of the males (M06, M11) were observed engaging in behaviour including genital sniffing (Fig. 1b, c) and grooming (Supplementary material), whilst the third male (M16) sat nearby. The interactions rotated frequently between the males over the 2 h (Fig. 1d). These behaviours were accompanied by high-pitched vocalisations characteristic of dependent back-young. After approximately 60 min, M11 moved to the other side of the canopy to feed, whilst M06 and M16 groomed each other for a further 60 min before separating to feed, at which point the observation was concluded.
Photographs of the three sub-adult male koalas engaging in apparently affectionate behaviour in Cape Otway, Victoria, 2015. (a) All three males interacting, (b) genital sniffing (M11 sniffing M06), (c) genital sniffing (M06 sniffing M16), and (d) genital sniffing (M16 sniffing M06). These behaviours were often accompanied by vocalisations characteristic of back young. A video of the M06 and M16 interaction can be seen in Supplementary material.
Interaction two
This interaction involved two of the three males above (M06, M11) and occurred over at least 40 min. The koalas were first observed immediately next to one another and consistently engaged in genital sniffing and intensive grooming throughout the interaction. No vocalisations were heard. After 40 min, M06 moved into the canopy of the neighbouring tree to feed, at which point I concluded the observation.
During the following 6 weeks, two of the three males dispersed from the study site; a behaviour typical of sub-adult males (Dique et al. 2003). M06 dispersed on 24 October and M11 dispersed on 3 November (Watchorn and Whisson 2019). Following their dispersal from the study site, their collars were removed and these individuals were no longer monitored. As such, their fate was unknown. M16 remained in the study area until the end of the study (December 2015).
Elevated hormonal activity in sub-adult animals can influence affiliative behaviours, play, boldness, and aggression, amongst other behaviours (Coe et al. 1981; Maggioncalda et al. 2002). However, the rarity of affiliative observations in koalas suggests that factors beyond sub-adult hormonal changes are driving these behaviours. One likely factor is population demography. The population in this study was founded by a bottlenecked island population and is characterised by low genetic diversity and an exceedingly overabundant population (15 koalas/ha) (Houlden et al. 1996; Melzer et al. 2000; Wedrowicz et al. 2018). The cause of overabundance is likely due to several interacting factors arising after the European invasion (Whisson and Ashman 2020), including: (1) low genetic diversity resulting from overexploitation and the severe genetic bottleneck (Menkhorst 2008); (2) reduced predation pressure, including from Traditional Custodians (Melzer et al. 2000; Yugovic 2015; Schlagloth et al. 2018); (3) habitat fragmentation inhibiting dispersal (Menkhorst 2008); and (4) the presence of certain food trees – particularly commercial blue gum (Eucalyptus globulus) plantations and woodlands dominated by swamp gum (E. ovata) and/or manna gum (Menkhorst 2008; Ashman and Watchorn 2019). These eucalypt species are high-quality food sources as they contain low levels of anti-herbivory compounds and high levels of available nitrogen and leaf moisture (Moore and Foley 2005). As such, koalas in these woodlands typically have small home ranges (<2 ha), exhibit high site fidelity, and are often reluctant to disperse to alternate habitat types even when trees become completely defoliated (Whisson et al. 2016; Watchorn and Whisson 2019).
Individuals with low genetic diversity can exhibit less aggression towards conspecifics (Barnard and Fitzsimons 1989; Tiira et al. 2003; Bubac et al. 2020; but see Ellison et al. 2013). For example, highly inbred mice exhibited less aggressive behaviour and were poorer competitors compared with males from outbred lines (Barnard and Fitzsimons 1989; Eklund 1996; Meagher et al. 2000). Similarly, land-locked juvenile salmon with closely related parents exhibited less aggression compared to more genetically diverse individuals (Tiira et al. 2003). However, the causal mechanism underlying these patterns can be difficult to disentangle (Tiira et al. 2003). While reduced aggression can be associated with low genetic diversity and the energetic costs of aggression (Barnard and Fitzsimons 1989), it could also be an indirect consequence of high relatedness within a population (e.g. kin recognition). These two factors are often correlated in small or isolated populations, making it challenging to isolate their independent effects. Whisson and Ashman (2020) hypothesised that koalas with low genetic diversity may better tolerate proximity to conspecifics, facilitating higher population densities. The three sub-adult males (M06, M11, M16) may share genetic information, which would support the contention; however, these data were not collected. Thus, as this hypothesis remains untested, it is unclear whether such tolerance is linked directly or indirectly to genetic diversity.
It is also possible, however, that non-aggressive and affiliative behaviours can improve the fitness of koala metapopulations, especially in high-density populations. In this population, home ranges (mean: 1.66 ha) were much smaller compared to lower-density populations elsewhere (8–118 ha) (White 1999; Ellis et al. 2002; Goldingay and Dobner 2013), and home range overlap among males was exceedingly high (Watchorn and Whisson 2019). Of the possible 55 male–male pairs, 46 (83.6%) had overlapping ranges (Watchorn and Whisson 2019). Therefore, male koalas in high-density populations may benefit from social affiliation behaviours to reduce conflict through familiarisation – a manifestation of the neighbourhood effect (Addicott et al. 1987). Such interactions may help to maintain stable dominance hierarchies, reducing the energy costs of aggressive encounters as males establish their home ranges (De Waal 1986; Addicott et al. 1987).
High-density populations can also increase social stress through heightened competition for resources like food, space, and mates (Creel et al. 2013). Grooming and other affiliative interactions, including vocalising, might alleviate stress, much like in other species where grooming plays a calming role (e.g. Shutt et al. 2007). Notably, female koalas have been observed engaging in social affiliation and homosexual interactions in captivity, even though only heterosexual copulations have been observed in the wild (Feige et al. 2007). These homosexual interactions comprised similar behavioural components as heterosexual interactions (Feige et al. 2007). The authors suggested that the behaviour may be a byproduct of the female-skewed, high-density population in the captive environment and act primarily as a form of stress release with minimal adaptive function, particularly given the absence of observations of the behaviour in wild populations (Feige et al. 2007). Similarly, the affiliative behaviours I observed may also be a stress-related by-product of an over-abundant population; however, copulatory behaviours – such as mounting, neck biting, thrusting, and bellowing – were not observed.
The behaviours reported here, and by Mitchell (1990a, 1990b), are likely byproducts of relatively extreme population demography. However, determining whether such behaviours are driven by the population’s poor genetic diversity, improvements to fitness via the neighbourhood effect, elevated stress, or a combination of these, is challenging due to the limited observations. Additionally, this study was not specifically designed to monitor the behaviour of sub-adult koalas, and as such these observations may not be representative of this wider population. For instance, five slightly younger sub-adult males (TWC 2) present in the population were not collared or monitored, despite their considerable body mass (mean: 6.9 kg). Tooth wear class estimates can also be somewhat subjective, particularly in conscious animals in field conditions, where detailed examination is challenging, and distinctions between classes (e.g. 2 and 3) may be minimal. While affiliative behaviour was only recorded in males, this may reflect the study design, as females were only observed when interacting with males (Watchorn and Whisson 2019). Notably, five sub-adult females (TWC 2–3) were also present in the study site. I strongly encourage further studies incorporating direct observation with proximity loggers (e.g. Ellis et al. 2015; Watchorn and Whisson 2019), analysis of genetic diversity and relatedness (e.g. Dennison et al. 2017; Schultz et al. 2020), and stress-hormone analysis (e.g. Narayan et al. 2013) to elucidate the prevalence of social affiliation behaviours in both high- and low-density koala populations.
Data availability
The observational data used to generate the results in the paper are not publicly available.
Declaration of funding
This project was funded in part by the Earthwatch Institute and the Field Naturalists Club of Victoria.
Acknowledgements
I wish to acknowledge the Gadubanud as the Traditional Custodians of the land on which this research was conducted. I thank Desley Whisson for her supervision and mentorship when this fieldwork was conducted, as well as for her comments on earlier versions of the manuscript. I also wish to thank Pat and the late Cyril Marriner for granting us access to the study site, and Katrina and Frank Fotinas of Bimbi Park for their logistical support. I thank the numerous volunteers who assisted with data collection, as well as Ross Goldingay and the anonymous reviewers for providing their valuable suggestions to improve the manuscript.
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