The role of acoustic and visual signals in species recognition in true lemurs (Eulemur: Primates)

Abstract

Signals represent important tools for animal social behavior. Numerous animal species use signals for communication as they serve as information transmitted from one individual to another. Signals also play essential roles in the evolution and the diversification of species as they can function for species recognition in several taxa. Additionally, they have evolved under several selective pressures such as natural selection through adaptation to natural habitats, sexual selection for species recognition or simply by random genetic drift. Several animal species including non-human primates use different species-specific signals to discriminate their own species from heterospecifics. Species recognition has been suggested to play an important role in order to avoid costly interbreeding, especially in female primates if they function as premating isolation mechanism. Primates can use different species-specific signals, such as olfactory, acoustic or visual signals, for species recognition. In lemurs, however, the use of species-specific signals for species recognition as well as the potentially selective factors influencing their evolution is largely unexplored. The aim of this thesis was to investigate the importance of acoustic and visual signals for species recognition in true lemurs (Eulemur taxa). To this end, I focused on wild redfronted lemurs (Eulemur rufifrons), which have a disjunct distribution in Madagascar and partly occur in sympatry with congeners. Males of the genus Eulemur exhibit high facial color variation and previous studies found small but significant differences in the acoustic structure of loud calls among Eulemur species. I therefore conducted playback experiments in two very different habitats in Madagascar (Kirindy Forest in the West and Ranomafana National Park in the East) in order to identify the role of acoustic signals such as loud calls for species recognition in E. rufifrons. Additionally, experiments using photographs of faces of different Eulemur species were conducted in Kirindy forest to test the ability of E. rufifrons for visual species recognition. Eulemur species used as stimuli in both experiments were composed of Eulemur rufifrons, E. rufus, E. fulvus, E. albifrons and E. rubriventer. I also aimed to identify the relative contribution of social and ecological factors to the diversification of facial color patterns in a comparative framework for the lemurs of Madagascar. To do so, I collected and analyzed photographs of 65 lemur species and ran phylogenetic comparative analyses in order to investigate the influence of social or ecological factors on the evolution of facial color patterns in lemurs. Results from playback experiments indicated that Eulemur rufifrons were not able to discriminate loud calls of their own species and closely related heterospecifics in both locations. However, animals were able to discriminate genetically distant E. rubriventer in Kirindy, but not in Ranomafana. Experiments using photographs of faces of different Eulemur species revealed that E. rufifrons were able to visually distinguish their own species from all heterospecifics. Additionally, their responses in terms of time looking towards the pictures were negatively correlated with genetic distance between the species used as stimuli. They also showed sniffing behavior that differed between each species stimulus. This again correlated negatively with genetic distance between the species stimuli. My phylogenetic comparative analyses indicated that social factors might have little or no influence on the evolution of facial color complexity in lemurs, whereas ecological factors might have marginally influenced the evolution of some facial regions. This part of my study also showed a strong effect of phylogeny on the evolution of color patterns in lemurs. The results of my thesis indicate that acoustic signals such as loud calls might play a less important role for species recognition in eulemurs, whereas visual signals such as facial color variation might be important for species recognition in order to avoid heterospecific mating. Diversification in acoustic signals of Eulemur rufifrons might be the result of random genetic drift, whereas both sexual selection and genetic drift might have influenced the evolution of facial color patterns in lemur species. This thesis has been the first comparative study investigating the evolution of facial color patterns in lemurs. It is also the first study conducting playback experiments and experiments using photographs in wild eulemurs to investigate their ability for species recognition using acoustic and visual signals. As there are many new questions that arose during the study concerning the evolution of signals in lemurs, my study opens several doors to explore the use and origin of signals in lemurs in more detail.