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Microsmatic primates revisited: Determining the importance of olfaction in primate communication

Final Report Summary - PRIMOLF (Microsmatic primates revisited: Determining the importance of olfaction in primate communication)

Summary description of the project objectives

Female primates signal impending ovulation with a suite of sexual signals. Studies of these signals focus on relationships among the signals, the timing of the fertile period, and male sexual behaviour. However, these studies have focused on visual, and to a lesser extent, acoustic signals, neglecting olfactory signals. Moreover, despite good theoretical reasons to expect that different modes of signalling communicate different information, to different male audiences, most studies to date have studied only one or two modes of signalling.

We aimed to investigate the information content of female olfactory signals in captive baboons (Papio anubis), and relate these to the female sexual cycle and the fertile period (determined using progesterone and estradiol levels, measured in saliva, as well as cytological evaluation of vaginal smears), other female sexual signals (acoustic, behavioural and visual), and male behaviour.

We used olive baboons (Figure 1), which are an excellent model species for this research project because they live in multi-male, multi-female groups in which females mate polyandrously.

The project had three major research objectives:
1. Olfactory signals and fertility. To conduct the first detailed chemical analyses of vaginal secretions in baboons and to investigate whether and how olfaction is related to female hormone levels (progesterone and estradiol) and the accuracy with which olfactory signals indicate the timing of ovulation and the fertile period.
2. Multiple signals: public and private information. To investigate whether and how other female signals (sexual behaviours, sexual swellings, copulation calls) interact with olfaction to indicate and conceal the timing of ovulation and the fertile period.
3. Male sexual behaviour, dominance status and female signals. To investigate the relationship between male sexual behaviour (inspections, mate-guarding, copulations) and female signals, to determine whether males use the different female signals to allocate their mating effort, and whether there are differences between males according to their dominance status.

Description of the work performed since the beginning of the project

We studied 15 baboons (three adult males and 12 adult females) living in four social groups housed at the French Research Council (CNRS) Primatology Station, Rousset-sur-Arc (France) (Figure 2).

First, we spent 10 weeks using positive reinforcement to train the female baboons to accept daily odour (vaginal secretions), cytology (vaginal smears) and sex hormone (saliva) sampling and collection of high quality images of sexual swellings (Figures 3 and 4). Next, we collected data for four months. We collected daily behavioural data for each female using 30 minute focal samples and collected odour, cytology and saliva samples daily on the same animals. We also used two camcorders and an additional external microphone to record behaviour. We made daily records of morphological changes in the anogenital area (sexual swellings) and menstruation. We used ad libitum records of submissive behaviour to determine female and male dominance ranks. At the end of the four months all individuals were captured and sedated to collect further data and samples (measures of the ischial callosities, standing height and weight, pure saliva and blood samples).

We measured sex hormone levels in saliva using enzyme-immuno assays at Durham Endocrinology and Ecology Laboratory, Durham University, Durham (UK). We prepared and stained vaginal smear slides using commercially available kits at the CNRS Molecular Biology Laboratory, and carried out cytological evaluation of slides in the School of Biological & Biomedical Sciences at Durham University. We conducted chemical analyses of odour at the Mass Spectrometry Center, Florence University and the Florence Research Area, Italian Research Council, Florence (Italy). We investigated the volatile component of odour signals using both solid-phase microextraction and dynamic headspace extraction followed by gas chromatography-mass spectrometry (GC-MS).

Description of the main results achieved so far

In total we obtained 1,872 digital images, 936 vaginal odour, 780 cytology and 390 saliva samples for 36 cycles (2-4 per female). We recorded all male and female sexual behaviours and vocalisations with a total of 329 hours of observations. We used vaginal cytology to detect ovulation (Figure 5). We identified a total of 66 volatile compounds (Figure 6), with many volatile fatty acids and hydrocarbons that have also been identified in GC-MS odour profiles for other mammals (including primates).

The training provided by Dr Setchell (scientist in charge) and Durham University (host institution) has contributed significantly to Dr Vaglio’s profile (research fellow), adding new methodological and scientific competences as well as complementary skills fundamental to his future career as an independent researcher. As a result, after the end of his Marie Curie Individual Fellowship, Dr Vaglio took up a permanent post as Lecturer in Animal Behaviour at University of Wolverhampton. He has been granted an Honorary Research Fellowship at Durham University to continue his research work with Dr Setchell.

Expected final results and their potential impact and use

We will address the research objectives by combining our measures of chemical signals (odour) with visual signals (sexual swelling characteristics, female sexual behaviour), observations of male sexual behaviour, and the timing of ovulation and the fertile period measured through objective criteria (vaginal cytology), to evaluate cycle-dependent changes in female signals, their reliability as indicators of the female fertile phase, and male response to these signals in captive olive baboons.

This study of olfactory signalling will provide a crucial missing piece of the puzzle of how females advertise their sexual receptivity. Results will determine whether these and other signal modalities provide different information concerning female fertility, and whether males differ in the quality of information available to them.

The project will contribute to our understanding of (i) olfactory communication in primates that, like humans, have traditionally been considered as “microsmatic”, (ii) the information that females provide to different males concerning their fertility, and (iii) the role of multiple signals in mate choice.

Contact details

Scientist in charge: Dr Joanna M. Setchell

Fellow Researcher: Dr Stefano Vaglio

Project public website