All in all, this study provides first empirical and quantitative information on the role of acoustic communication for spacing and cohesiveness in the woolly lemur as a representative of the nocturnal pair-living primates. As in their diurnal relatives, acoustic signaling represents an important mechanism to regulate distances between pairs in space and to maintain cohesion between pair partners. A more sophisticated acoustic analysis of the vocalizations of woolly lemurs and playback experiments are now urgently needed to explore to which extent woolly lemurs use and perceive the messages acoustically conveyed in their calls. Furthermore, as loud calls are often used successfully to assess taxonomic and phylogenetic relations or migrations patterns in other primates (Davila Ross and Geissmann 2007; Méndez-Cárdenas et al. 2008; Meyer et al. 2012), it would be interesting to examine the use of loud calls for conservation purposes in this endangered lemur species. Woolly lemurs are known to develop prominent scent glands under the chin (Warren and Crompton 1997).
Further investigations are thus needed to explore to which extent woolly lemurs use olfactory signalling for communication.
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Chapter 5 GENERAL DISCUSSION
CHAPTER 5
GENERAL DISCUSSION
The study of sociality and communication is a major topic in behavioural ecology. It provides important insights into the interplay of the ecological determinants of sociality.
Individuals live in social networks characterized by sleeping groups, interactions through vocalizations and/or scent-marking and occasional encounters at night (e.g. CHARLES-DOMINIQUE 1977, 1978; BEARDER 1987). Here, I will discuss the significance of sleeping site ecology for the conservation of primates, and woolly lemurs in particular. Furthermore I will compare my findings on sociality and communication with those on other related primate species to embed my findings on woolly lemurs into our current knowledge of the family Indriidae. Based on that, I will put forth perspectives for future research.
Sleeping site ecology in primates and its significance for conservation
In chapter 2, I have demonstrated that sleeping sites are a potentially limited resource for woolly lemurs, especially during the dry season, and that sleeping site ecology varies according to season. During the late dry season, woolly lemurs often reused the same sleeping site and preferred to sleep at the height of 5-10 m. My findings suggest that western woolly lemurs are particularly conspicuous for hunters during the dry season since they are at an accessible height for humans. They are uncovered, obvious to hunters, and can be picked up by hand without the need for weapons (GARCIA u. GOODMANN 2003). Habitat requirements of species may determine their vulnerability to anthropogenic disturbance.
Many kinds of primates use nests, tree holes or hollows, and open vegetation for sleeping site (e.g. RADESPIEL et al. 1998, BEARDER et al. 2003, RADESPIEL et al. 2003, RASOLOHARIJAONA et al. 2003, SCHÜLKE AND KAPPELER 2003, RASOLOHARIJAONA et al. 2008, BIEBOUW et al. 2009). They require a special physical characteristic on their sleeping tree to allow them to stay safely during their long resting time.
For example, arboreal primates sleeping in open vegetation tend to select trees with large diameters and large crown (e.g. VON HIPPEL, 1998; DI BITETTI et al. 2000; LI et al. 2006;
CUI et al. 2006; FAN u. JIANG 2008; XIANG et al. 2010). Living in a harsh environment, monkeys preferred tall conifers at middle slopes (CUI et al. 2006). Information about the characteristics and usage of sleeping sites helps in conservation planning and the restoration of habitat (PLUMPTRE u. REYNOLDS 1997; BLOM et al. 2001; JOHNSON et al. 2004).
In defoliated trees, primates are easily detectable making the animal using the trees for concealment vulnerable to predators and hunters (PEETZ et al. 1992). Humans are among the
Chapter 5 GENERAL DISCUSSION predators of animals. Many primate populations are severely threatened by human activities (WILSON u. WILSON 1975; HAMILTON et al. 1986; WHITE u. OATES 1999;
COWLISHAW u. DUNBAR 2000). In the gray monkeys, for example, humans were likely the primary predators (XIANG et al. 2009). In a remote forest of western Brazilian Amazonia, more than 80 woolly monkeys, spider monkeys and howlers were killed by a single family of rubber tapers (Peres 1990). Hunting may have played a part in the extinction of some Malagasy lemurs (PEREZ et al. 2005). It may be more widespread than previously thought and deserves urgent attention from conservationists. Even though all lemur species are protected, participation in hunting of protected species is widespread. Around the world, hunting is the second most important threat to primate populations behind the loss of habitat (MITTERMEIER et al. 2006). It is a serious threat to long-term conservation and species survivorship. Thus, hunting and habitat destruction and degradation threaten the survival of many primate species (SANDERSON et al. 2002).
My data suggests that arboreal primates sleeping in open vegetation are easy to find and to catch in the dry season when trees are leafless. My findings have significant implications for forest management. Based on my results and analysis, I make the following management recommendations for the conservation of arboreal primates. We need to identify the characteristics of the sleeping trees potentially important for the arboreal species, for example large trees with dense coverage. Conservation management strategies should ensure the maintenance of these trees and suitable habitats necessary to the survival of the animals.
Furthermore, the management of the reserve or park should monitor illegal poaching by increased patrolling and law enforcement, and carry out an education program involving conservation awareness to ensure that villagers do not kill the animals. Parks and reserves should maintain better monitoring of the forest, particularly during the dry season, to guarantee the future survival of the animals. Further research into sleeping tree availability should enable a better assessment of the conservation needs of these species. Indeed, there may well be other cues, not measured in my study, that are important for arboreal primates.
The lack of information on habitat requirements of some arboreal primates precludes well-informed management decisions and further research is clearly required.
Social systems and social relations within Indriidae
Woolly lemurs are the only taxa among nocturnal strepsirrhines living in family groups (THALMANN 2001). In the family of Indriidae to which woolly lemurs belong, the
other taxa (Propithecus, Indri) live either as pairs, in small family groups or in multi-male multi-female systems. Living in pairs or small family groups may reduce mortality and increase foraging success. Food items as well as sleeping sites are patchily distributed for woolly lemurs, especially in the dry season (THALMANN 2001; RAMANANKIRAHINA et al. 2012). It might be therefore advantageous for both male and female woolly lemurs to share their range with a familiar mate to avoid predation and defend territories. Because predation results in death, selection to avoid it must be very strong. Moreover, males are unable to maintain territories that can support more than one female if females are so widely distributed in space. They have a small body size and low energy diet. They are forced into pair living as energy-saving strategy (NORSCIA u. BORGOGNINI-TARLI 2008). Furthermore, most folivourous mammals are diurnal, woolly lemurs are thus assigned to secondary nocturnal habits like in Aotus, the only nocturnal anthropoid (GANZHORN et al 1985; MARTIN 1990).
The pressures of predators (Hawks and Eagles) are suggested to explain the nocturnal activity in Aotus. Thus, living-group may be the ancestral characteristic in woolly lemurs, retained from a diurnal activity pattern (GANZHORN et al 1985).
Despite its nocturnal activity, the western woolly lemurs show the same pattern of pair relations as their diurnal relatives living in either pairs or multi-male multi-female systems.
Unambiguous female dominance (agonistic superiority of the female over males across different contexts) was reported for the diurnal species of the socially cohesive lemurs of the family Indriidae (POLLOCK 1979; MEYERS 1993; POCHRON et al. 2003). The degree of female dominance is variable among the lemurs and described to be affected by social system and activity pattern (RADESPIEL u. ZIMMERMANN 2001). Female dominance is a rare trait in social systems of mammals and within primates, but seems to be widespread among the lemurs of Madagascar (DUNHAM 2008). The direction of aggressive or submissive behaviours in agonistic encounters and the outcome of intersexual conflicts are frequent measures of dominance. In western woolly lemurs, affiliative behaviours are considerably more common than agonistic behaviours. Male and female partners interacted peacefully.
Agonistic behaviour was rarely observed and always initiated by the female. According to the definition of dominance (RADESPIEL u. ZIMMERMANN 2001) females of the western woolly lemurs showed unambiguous dominance over males, meaning dominance across different contexts. Females won every decided intersexual conflict. Males exhibited submissive behaviours to their mates in the absence or presence of aggressive behaviour from females. Thus, female dominance is not linked to activity pattern and social system, but is an
Chapter 5 GENERAL DISCUSSION ancestral trait originating from a common ancestor. In order to better understand the evolution of female dominance, more empirical and quantitative studies on the context, distribution and outcome of intersexual relationships are needed.
Mechanisms regulating inter- and intra-pair spacing: acoustic communication
Individuals interact physically and vocally. In chapter 4, I have demonstrated that western woolly lemurs depend on acoustic signalling to maintain contact and to manage intra- and inter- pair interaction. From my findings, Avahi produces loud calls for resource/territorial defence and aggregation of group. Mate defence or mate attraction did not appear to be the function of the loud calls in western woolly lemurs. The vocal rate of the loud calls did not increase during the dispersal or mating season. Male and female produced the long distance calls with the same rate, which is in contrast with the mate defence announce their presence within the territory, and to make information available about their location and distance. However, Indri use song or duets for territorial defence (THALMANN et al. 1993, GEISSMANN u. MUTSCHLER 2006). A duet was not found in my study of woolly lemurs. Patel (2010) does not record any call functioning for a territorial defence in their study on Propithecus candidus. However, PETTER u. CHARLES-DOMINIQUE (1979) reported that Propithecus sp. utter a barking call for distant communication between groups.
They are often associated with territorial confrontations and evoke counter-calling from neighbouring groups. Propithecus are also reported to use scent-marking for territorial defence (e.g. POCHRON et al. 2005). Western woolly lemurs have marked trees during my follows but the functions of this behaviour remain unknown. This means that acoustic signals might not be linked to phylogenetics since Indri, Propithecus and Avahi show very different ways of communicating.
Western woolly lemurs ultimately remain spatially cohesive by means of calling. They use loud calls, whistles, to maintain and coordinate movements when they are separated. The loud calls seemed to serve as contact calls that maintained group cohesion and prevented individuals from becoming lost. In contrast, Indris use a low-pitched and low intensity
vocalization to maintain close contact with the group during resting activities or group displacements (MARETTI et al. 2010). Propithecus use low amplitude, tonal, and very low frequency contact calls during group movement and in a variety of circumstances such as affiliation, foraging and while resting (PATEL 2010). Indri and Propithecus use a short distance communication call to permit the animals to remain in contact during locomotion.
Additionally, Propithecus possesses one call (howl) that they emit when individuals become spatially separated from the group which could act in the same way as the whistle call in Avahi. However, howl calls get always another type of call (Zzuss) in response from group members which is the same as the whistle call. Thus, it seems that western woolly lemurs do not show similar patterns of communication as their family relatives when remaining in contact with member of groups, confirming our statement above that acoustic signal might not be linked to phylogenetics.
In the presence of other species, western woolly lemurs produce the growling call, a soft and noisy call consisting of rapidly repeated, short, broadband pulses, used as a threatening call. This is a no predatory event. In Propithecus, they do emit purr call towards human observers, acting as low-level threat vocalization. In Indris, there is no similar vocalization but in response to disturbances, they reacted with calls of medium intensity
In the presence of other species, western woolly lemurs produce the growling call, a soft and noisy call consisting of rapidly repeated, short, broadband pulses, used as a threatening call. This is a no predatory event. In Propithecus, they do emit purr call towards human observers, acting as low-level threat vocalization. In Indris, there is no similar vocalization but in response to disturbances, they reacted with calls of medium intensity