Stefano Vaglio

Odour signals major histocompatibility complex genotype in an Old World monkey

The major histocompatibility complex (MHC) is an extraordinarily diverse cluster of genes that play a key role in the immune system. MHC gene products are also found in various body secretions, leading to the suggestion that MHC genotypes are linked to unique individual odourtypes that animals use to assess the suitability of other individuals as potential mates or social partners. We investigated the relationship between chemical odour profiles and genotype in a large, naturally reproducing population of mandrills, using gas chromatography–mass spectrometry and MHC genotyping. Odour profiles were not linked to the possession of particular MHC supertypes. Sex influenced some measures of odour diversity and dominance rank influenced some measures of odour diversity in males, but not in females. Odour similarity was strongly related to similarity at the MHC, and, in some cases, to pedigree relatedness. Our results suggest that odour provides both a cue of individual genetic quality and information against which the receiver can compare its own genotype to assess genetic similarity. These findings provide a potential mechanism underlying mate choice for genetic diversity and MHC similarity as well as kin selection.

Chemical Composition of Scent-Gland Secretions in an Old World Monkey (Mandrillus sphinx): Influence of Sex, Male Status, and Individual Identity

Primates are traditionally considered to be microsmatic, with decreased reliance on olfactory senses in comparison to other sensory modalities such as vision. This is particularly the case for Old World monkeys and apes (catarrhines). However, various lines of evidence suggest that chemical communication may be important in these species, including the presence of a sternal scent-gland in the mandrill. We investigated the volatile components of mandrill odor using gas chromatography-mass spectrometry. We identified a total of 97 volatile components in 88 swabs of the sternal gland secretion and 95 samples of sternal gland hair saturated with scent-gland secretion collected from 27 males and 18 females. We compared odor profiles with features of the signaler using principle components and discriminant function analyses and found that volatile profiles convey both variable (age, dominance rank in males) and fixed (sex, possibly individual identity) information about the signaler. The combination of an odor profile that signals sex, age, and rank with increased motivation to scent-mark and increased production of secretion in high-ranking males leads to a potent signal of the presence of a dominant, adult male with high testosterone levels. This may be particularly relevant in the dense Central African rain forest which mandrills inhabit. By contrast, we were unable to differentiate between either female cycle stage or female rank based on odor profiles, which accords with behavioral studies suggesting that odor signals are not as important in female mandrills as they are in males. The similarity of our findings to those for other mammals and in primates that are more distantly related to humans suggests a broader role for odor in primate communication than is currently recognized.

Volatile Signals During Pregnancy: A Possible Chemical Basis for Mother–Infant Recognition

Human pheromones play a role in regulating relationships and apparently influence partner choice and mother–infant recognition. We analyzed the chemical content of volatiles from sweat patch samples from the para-axillary and nipple–areola regions of women during pregnancy and after childbirth. Solid phase microextraction was used to extract the volatile compounds, which were then characterized and quantified by gas chromatography–mass spectrometry. During pregnancy, women developed a distinctive pattern of five volatile compounds common to the para-axillary and nipple–areola regions (1-dodecanol, 1-1′-oxybis octane, isocurcumenol, α-hexyl-cinnamic aldehyde, and isopropyl myristate). These compounds were absent outside pregnancy and had slightly different patterns in samples from the two body areas. Differentiation of the volatile patterns among pregnant women may help newborns to distinguish their own mothers.

Chemical communication and mother-infant recognition

Fifty years after the term ‘pheromone’ was coined by Peter Karlson and Martin Lüsher, the search for these semiochemicals is still an elusive goal of chemical ecology and communication studies. Contrary to what appears in the popular press, the race is still on to capture and define human scents. Over the last several years, it became increasingly clear that pheromone-like chemical signals probably play a role in offspring identification and mother recognition. Recently, we analyzed the volatile compounds in sweat patch samples collected from the para-axillary and nipple-areola regions of women during pregnancy and after childbirth. We hypothesized that, at the time of birth and during the first weeks of life, the distinctive olfactory pattern of the para-axillary area is probably useful to newborns for recognizing and distinguishing their own mother, whereas the characteristic pattern of the nipple-areola region is probably useful as a guide to nourishment.

Sternal Gland Scent-Marking Signals Sex, Age, Rank, and Group Identity in Captive Mandrills.

Mandrills are one of the few Old World primates to show scent-marking. We combined ethological and chemical approaches to improve our understanding of this behavior in 3 zoo-managed groups. We observed the olfactory behavior performed by adults and adolescents (N = 39) for 775h. We investigated the volatile components of sternal scent-marks using gas chromatography-mass spectrometry and compared volatile profiles with traits of the signaler. Males marked more than females and within each sex the frequency of scent-marking was related to age and dominance status, but alpha males scent-marked most frequently and particularly in specific areas at the enclosure boundaries. We identified a total of 77 volatile components of sternal gland secretion, including compounds functioning as male sex pheromones in other mammals, in scent-marks spontaneously released on filter paper by 27 male and 18 female mandrills. We confirmed our previous findings that chemical profiles contain information including sex, male age and rank, and we also found that odor may encode information about group membership in mandrills. Our results support the hypotheses that scent-marking signals the status of the dominant male as well as playing territorial functions but also suggest that it is part of sociosexual communication.

Red-green color vision in three catarrhine primates.

The evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, specifically the detection of either ripe fruits or young leaves amid mature foliage, and to the intraspecific socio-sexual communication, namely the signal of the male rank, the mate choice and the reproductive strategies in females. New data should be added to the debate regarding the evolution of trichromatic color vision. Three catarrhine primates were observed to achieve this goal. The research was performed on captive groups of vervet monkeys (Chlorocebus aethiops), pig-tailed macaques (Macaca nemestrina) and chimpanzees (Pan troglodytes) housed at Parco Natura Viva - Garda Zoological Park (Italy). Using pairs of red-green bags containing the same hidden reward in comparable outdoor enclosures, we recorded the choices by observed individuals (n = 25) to investigate the role of color cues in choosing an object. The results indicate that chimpanzees used red color as cue to choose an object that contains food by showing a preference toward red objects; in contrast, vervet monkeys and pig-tailed macaques do not demonstrate a clear choice based on the color of the object. Our findings highlight the importance of the foraging hypothesis but not rule out the potential role of the intraspecific socio-sexual communication and may serve to add useful information to the debate regarding the adaptive value of the evolution of color vision in order to fill a phylogenetic gap from Old World monkeys to humans. Future studies should address the role of socio-sexual communication, such as the selection of the reproductive partner of both high genetic quality and with compatible genes, to determine how this influenced the evolution of color vision in non-human primates.

Fecal Concentrations of Cortisol, Testosterone, and Progesterone in Cotton-Top Tamarins Housed in Different Zoological Parks: Relationships Among Physiological Data, Environmental Conditions, and Behavioral Patterns

The aim of this investigation was to study the welfare of 3 captive groups of cotton-top tamarins housed in different zoological parks. Ethological observations were conducted during 1 year. In addition, fecal samples were collected and the concentrations of glucocorticoids, androgens, and progestogens were measured. Within each group, no significant differences in fecal cortisol concentrations were found between subjects. The fecal concentrations of testosterone and progesterone significantly differed depending on the sexes and ages of the tamarins. A significant association was found among hormone concentrations, exhibit dimensions, and group composition. A highly significant correlation was found between all hormones considered and the space available for each subject. Significant differences in behavioral patterns were observed among groups, including social–individual, affiliative–aggressive, and anogenital–suprapubic scent marking. Correlations between hormone measurements and behaviors were detected. In conclusion, this study confirmed the associations between some behaviors exhibited by these nonhuman primates and both cortisol and testosterone; these data also highlight the role played by progesterone in these behaviors.

Positive reinforcement training : a tool for care and management of captive vervet monkeys (Chlorocebus aethiops).

In modern zoos, training should be an integral component of the animal care and management. The benefits of training include the opportunity for positive interactions with caretakers. This study was carried out with a group of vervet monkeys (Chlorocebus aethiops) housed at the Garda Zoological Park (Italy). Using focal animal sampling, we observed the behaviour performed by all group members (N = 10) from December 2007 to August 2008. The group took part in a training program to be isolated in a familiar area before the subjects were included in a cognitive study. We collected behavioural data during a pre-training period to assess the social behaviour of the colony and during the training period to investigate the effects of the training program on the behaviour of individuals. Additionally, a second phase of the study was conducted and training sessions with individual monkeys were video-recorded to determine the behaviour of animals during each training session and thus to confirm that they were suitable for participating in the procedure. Our results suggest that the training program enriched the daily routine of these captive primates by increasing affiliative behaviours while decreasing agonistic behaviours. Furthermore, there was behavioural response variability among the individuals under training procedure. However all the individuals were trained to calmly enter in a familiar area and to be isolated from other members of the group. In conclusion, our findings highlight the importance of using the positive reinforcement training to reduce the tension directly associated with potentially stressful procedures by allowing primates to voluntarily participate in these procedures. In addition, the training was found to be an enrichment tool for vervet monkeys.

Volatile Signals during Pregnancy

Scents play a key role in mediating reproductive interactions in many vertebrates including mammals. Nowadays, several studies indicate that humans seem to use remarkably olfactory communication and are even able to produce and perceive pheromones. Furthermore, over the past several years, it became increasingly clear that pheromone-like chemical signals probably play a role in offspring identification and mother recognition. Recently developed technical procedures (solid-phase microextraction and dynamic headspace extraction) now allow investigators to characterize volatile compounds with high reliability. We analyzed the volatile compounds in sweat patch samples collected from the para-axillary and nipple-areola regions of women during pregnancy and after childbirth. We hypothesized that, at the time of birth and during the first weeks of life, the distinctive olfactory pattern of the para-axillary area is probably useful to newborn babies for recognizing and distinguishing their own mother, whereas the characteristic pattern of the nipple-areola region is probably useful as a guide to nourishment.

Histology of the Suprapubic and Anogenital Cutaneous Glands in Male Cotton Top Tamarins (Saguinus oedipus)

In cotton top tamarins (Saguinus oedipus), scent glands have been mostly studied in females from museum collections. This work aims to extend the investigation to male specimens, introducing a novel source of skin samples. Two adult males from zoo populations, one intact and one castrated, were immediately frozen after natural death. Skin samples were later collected at the thawing onset, soaked with cold fixative and processed for light microscopy. Sebaceous units of scent glands showed phasic secretory activity in the intact male and marked fibrosis in the castrated male. It appears, therefore, that light microscopy samples from frozen tissues provide detailed features that can disclose distinctive traits in specimens characterized by different hormonal balances.