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Digital archive of theses discussed at the University of Pisa


Thesis etd-12092009-111223

Thesis type
Tesi di dottorato di ricerca
Thesis title
Back to Prosimians: new evidence on play behaviour and its possible adaptive roles
Academic discipline
Course of study
tutor Prof.ssa Borgognini Tarli, Silvana
  • Berenty reserve
  • Foreigners
  • Grooming
  • Ice-breaker mechanism
  • Lemur catta
  • Play behaviour
  • Propithecus verreauxi
  • Social behaviour
  • Tolerance
Graduation session start date
Release date
Play can be defined as all activity that appears to an observer to have no obvious immediate benefits for the performer, but which involves motor patterns typical of serious functional contexts, such as agonistic, anti-predatory, and mating behaviour (Martin & Caro 1985; Pellis & Pellis 1996; Bekoff 2001; Burghardt 2005). In juveniles play seems to have a role in developing and training motor skills by enhancing musculoskeletal development and cardiovascular system (Byers & Walker 1995) and by practising specific survival skills (Spinka et al. 2001). However, social play can be also fruitful at an immediate level in manipulating and testing social relationships (Breuggeman 1978; Drea et al. 1996; Palagi 2009), reducing tension (Palagi et al. 2004, 2006, 2007), and increasing social cohesiveness (Thompson 1998).
Play challenges psychologists to discover its consequences on behavioral development, anthropologists to identify its role in the evolution of social and cognitive skills, and evolutionary biologists to search for the functions of an apparently nonfunctional behavior (Burghardt, 2005). Even though we are far from a satisfactory knowledge-level on play, in the last two decades many efforts have been made to better understand and clarify some aspects of this behavior. Indeed, most of these efforts were especially focused on the potential meaning of play behavior.
Play is a multifunctional phenomenon because its roles may vary according to a number of different factors such as species, age, sex, and relationship quality of the players. For this reason, a comparative approach in the study of animal play is needed to rigorously assess the relative importance of different functions of play for different species (Fagen 1981).
To date, within Primates, the research on play behaviour has mostly focused on Haplorhines rather than Strepsirhines that have been almost completely neglected.
Lemurs, which are relatively small brained, form an independent primate radiation and represent the most primitive group-living primates (Armstrong 1985; Tattersall 1982). Moreover, some lemur species share common features with many Haplorhines species, such as the diurnal habit, high level of sociality and the presence of visual communication (Jolly 1966; Pereira et al 1988; Palagi 2009). Altogether, these characteristics represent the basis for the study of play behaviour, particularly for social play (the most sophisticated form of play). In this perspective, investigation within lemur species may represent an opportunity for looking for possible adaptive roles of such complex behaviour.
I selected ringtailed lemurs (Lemur catta – family Lemuridae) and sifaka (Propithecus verreauxi – family Indridae) as model species in this study for the following reasons:
 The two species live in sympatry in the study-site, consequently the data collection was not affected by any difference in external environmental pressures. Moreover, the data considered for this study were collected for both species in the same season, the wet season.
 The two species are diurnal and lives in multimales/multifemales groups where each sex and age classes are represented, thus allowing the analyses on social play in this respect.
 Although the two species are phylogenetically close-related, they show species-specific differences in several behavioural features, such as the social structure in terms of inter-individual relationships and level of despotism.
The goal of the study is to deeply investigate the use of play behaviour within ringtailed lemurs and sifaka according to their species-specifics behavioural features in order to add key-interpretations on play and its possible functions and adaptive roles.
Here I first put in relation play behaviour with the striking different habitat exploitation, anatomical and locomotion constraints shown by the two study species. Indeed, ringtailed-lemur is the most terrestrial lemur (mainly using quadrupedal locomotion) and sifaka one of the most arboreal one (mainly using clinging and leaping locomotion habits).
Secondly, I based the research analyses on social behaviour features shown by the two study species.
Ringtailed lemurs live in a prominent despotic society expressed by: i) inter-individual relationships, which are strongly codified according to rank rules (Kappeler 1990; Palagi et al 2005); ii) the presence of relatively diverse set of signals and ritualization, usually used for maintaining unambiguous, public dominants relationships (Submissive Spat-Grimace, Yawning and Gnashing, then Stink fight); ii) high level of territoriality, making ringtailed lemurs groups completely “sealed” to outsiders (Huntingford &Turner 1987; Beckoff 1975, 1977).
Conversely sifaka live in a more tolerant society expressed by: i) female dominance over males, translated more into feeding priority than into general despotic relationships (Richard 1974); ii) absence of ritualization or meta-communication signals; ii) living in permeable groups, particularly during the mating season when outgroup males visit other groups for mating purposes (Brockman and Whitten 1996; Brockmann 1999; Ostner & Kappeler 2004; Norscia et al. 2009).
In this perspective, if play is a multifunctional phenomenon because its roles may vary according to a number of different factors such as species, age, sex and inter-individual relationship among players (Fagen 1981; Burghardt 2005; Palagi 2006, 2008, 2009; Palagi et al. 2007), I expect to find different functions in the use of play within the two species. Moreover, due to the natural territorial overlapping characterizing the study site, if play is used as a means for copying with “social novelty”, I expect to find within each species a different use of such means in presence of external lemur groups.
I conducted this study in the Ankoba secondary forest (40-ha) of the Berenty Reserve in Southern Madagascar. The site is characterized by two main climatic periods: the wet season (from October to March) and the dry season (from April to September) (Jolly et al. 2006). At Berenty, ringtailed lemurs and sifaka live in sympatry with another species (showing cathemeral habits) the brown lemurs (Eulemur fulvus). The three species naturally have overlapping ranges and dietary so they likely compete for similar foods during times of scarcity (dry season).
I collected data during two different periods to cover the two seasons:
- First period of observation – wet season (Nov 2006 – Feb 2007). I observed 2 groups of ringtailed lemurs composed by 9 individuals (4 adult males, 1 infant male, 3 adult females and 1 sub-adult female) and 16 individuals (4 adult males, 2 sub-adult males, 2 infant males, 6 adult females, 1 sub-adult female and 1 infant female) respectively. I observed 2 groups of sifaka composed by 8 individuals (5 adult males, 2 adult females, 1 sub-adult female) and 6 individuals (1 adult male, 2 sub-adult males, 2 adult females and 1 sub-adult female) respectively. In addition, I also collected standardized data on 9 outgroup males started visiting my study groups two months after the beginning of the observations and one month before the first mating day (Norscia et al. 2009).
- second period of observation – dry season (Mar 2008 – Jul 2008). I observed 2 groups of ringtailed lemurs composed by 13 individuals (4 adult males, 1 juvenile male, 4 adult females and 2 juvenile females) and 19 individuals (5 adult males, 3 infant males, 8 adult females and 3 infant females) respectively. For sifaka, I observed the same groups of the previous observational period; nevertheless I found some changes in group composition. The two groups of sifaka were composed by 8 individuals (3 adult males, 1 sub-adult males, 3 adult females and 1 juvenile female) and 7 individuals (2 adult males, 2 juvenile males, 2 adult females and 1 juvenile female) respectively.
Behavioural data have been collected basing on ethograms that include solitary and social behaviours (affinitive, aggressive, submissive and neutral items).
For data collection I used focal animal sampling, all occurrences and ad libitum methods (Altman 1976).
- focal sampling. For ringtailed lemurs a total of 729h of observation (400 for the first and 329h for the second observational period) has been collected. For sifaka a total of 1.019h of observation (501h for the first and 518h for the second observational period) has been collected.
- All occurrences. For ringtailed lemur a total of 831h of observation (350 for the first and 481h for the second observational period of observation) has been collected. For Sifaka a total of 653h (273h for the first and 380h for the second observational period of observation) has been collected.
Since the number of play session occurred during the second period of observation (dry season) was low (only 2 sessions for ringtailed lemurs and 14 for sifaka), I focalised the data analyses only on the first period of data collection.
I used nonparametric statistical tests (Siegel & Castellan, 1988; Lehener, 1996; Zar, 1999) for data processing.
Results and discussion
The occurrence of play in sifaka and ringtailed lemurs at different forest layers seems to be related to their anatomical and locomotion constraints, and habitat exploitation.
Within ringtailed lemurs play occurs also among adults other than immature individuals. Here, I show that play mostly occurs among subordinates individuals (adult males and sub-adults); whereas low levels of play occur among high-ranking females whose dominance is stable and unquestionable. Therefore, play seems to be used by ringtailed lemurs as an “informative and safer tool” for those individuals who need to improve their fighting abilities and assess the strength/weakness of possible competitors. Such tool seems to be helpful in improvement of dominant status (peripheral males to become “prime”, sud-adult females minimizing the risk of being “targeted”) (“social assessement hypothesis” Geist 1982; Jones 1983; Pellis et al. 1993; Paquette 1994).
Moreover, the presence of relatively diverse set of signals and ritualization are predictive of a despotic society (Huntingford &Turner 1987; Beckoff 1975, 1977). Such signals are used to maintain unambiguous, public dominants relationships (Submissive Spat-Grimace, Yawning and Gnashing, then Stink fight). Ringtailed lemurs use their tail as a signals of communication in different aspects of social life, such as agonistic, marking and play behaviour. In particular, “anoint tail” (olfactory signal) and “wave tail” (visual signal) are used in different combinations both in agonistic and playful contexts toward competitors or playmates (Jolly 1966; Palagi 2009). Here I provide evidence on the use of play signals (tail play) which have been retained for playful activity (tail-play) to avoide “misinterpretation” during the riskiest form of play (rough play). In particular, as stink fight are used in dyadic aggressive encounters, I proved that tail play reaches the most effectiveness during dyadic play.
In addition, during polyadic play sessions, play itself seems to be a means for signalling the “social status” and maintaining the play session, thus explaining the decreased level of tail play found in polyadic sessions.
Finally, the high level of despotism, expressed also by high level of territoriality, makes ringtailed lemur completely “sealed” to outsiders. No “intruders” are admitted into the group without engaging in overt fights beforehand (Jolly 1966). In presence of possible food competitors represented by conspecifics or alien species play seems to have been retained for two possible roles: realising stress of group-members during mild stress situation (Pellis 2002) or, once more, as an “honest signal” for convey information towards competitors about the proper aggressive intent and/or the fighting ability (the “Zahavi’s handicap principle” - Zahavi 1975).
On the other hand, sifaka live in a more tolerant society compared to ringtailed lemurs. Within this species I found evidence that play has not be retained into adulthood for courtship purposes (the observational period fall into the mating season). On the contrary, non-sexual play is expressed for coping with the onset of novel social circumstances: the presence of temporary outgroup males. Indeed, play seems to be a means to test emergent relationships between unfamiliar individuals and can work as a signal of non-agonistic intent in a sort of short-range communication and/or as a means for social and self-assessment. In presence of possible social tension induction (mild stress condition) due to the presence of new individuals, sifaka seem to use play for stress realising. The lack of meta-communication signals reflects the difficulty to maintain the playful mood without incurring in a high risk of aggression, so that sifaka males adjust their playful tactics as a function of playmates’ group membership while playing longer with residents in the riskiest form of play (rough play). Finally, play while arising spontaneously, independently from the presence of previous affinitive behaviour with unfamiliar individuals suggests that play it may represent a bridge between the two unfamiliar subjects. In conclusion, by the light of results found, here I propose a new possible hypothesis of play behaviour: “the ice-breaker hypothesis”; that is play functions as a mechanism which enhances friendly interactions in the critical process that leads a “stranger” to become “familiar”.