Males are more sensitive to their audience than females when scent-marking in the redfronted lemur

Audience effects, i.e. changes in behaviour caused by the presence of conspecifics, have rarely been studied in the context of olfactory communication, even though they may provide important insights into the functions of olfactory signals. Functional sex differences in scent-marking behaviours are common and influenced by the social system. To date, patterns of functional sex differences in scent-marking behaviours remain unknown in species without overt dominance relationships. We investigated sex differences in intra-group audience effects on anogenital scent-marking in a wild population of redfronted lemurs (Eulemur rufifrons) by performing focal scent-marking observations. With a combination of generalised linear mixed models and exponential random graph models, we found different audience effects in both sexes. Males were overall more sensitive than females to their audience. Only males seemed to be sensitive to the presence of both members of the opposite sex and same-sex conspecifics in the audience. Females were only moderately sensitive to the presence of other females in the audience. This study offers a potential behavioural pattern associated with anogenital scent-marking that seem to differ from those described for species exhibiting female dominance, supporting the notion that the social systems co-varies with scent-marking behaviours and scent-complexity in strepsirrhines.

Assessing urinary odours across the oestrous cycle in a mouse model using portable and benchtop gas chromatography-mass spectrometry

For female mammals, communicating the timing of ovulation is essential for reproduction. Olfactory communication via volatile organic compounds (VOCs) can play a key role. We investigated urinary VOCs across the oestrous cycle using laboratory mice. We assessed the oestrous stage through daily vaginal cytology and analysed urinary VOCs using headspace gas chromatography-mass spectrometry (GC-MS), testing a portable GC-MS against a benchtop system. We detected 65 VOCs from 40 samples stored in VOC traps and analysed on a benchtop GC-MS, and 15 VOCs from 90 samples extracted by solid-phase microextraction (SPME) and analysed on a portable GC-MS. Only three compounds were found in common between the two techniques. Urine collected from the fertile stages of the oestrous cycle had increased quantities of a few notable VOCs compared with urine from non-fertile stages. These VOCs may be indicators of fertility. However, we did not find significant differences in chemical composition among oestrous stages. It is possible that changes in VOC abundance were too small to be detected by our analytical methods. Overall, the use of VOC traps combined with benchtop GC-MS was the more successful of the two methods, yet portable GC-MS systems may still have utility for some in situ applications.

Flow-mediated olfactory communication in honeybee swarms

Honeybee swarms are a landmark example of collective behavior. To become a coherent swarm, bees locate their queen by tracking her pheromones. But how can distant individuals exploit these chemical signals, which decay rapidly in space and time? Here, we combine a behavioral assay with the machine vision detection of organism location and scenting (pheromone propagation via wing fanning) behavior to track the search and aggregation dynamics of the honeybee Apis mellifera L. We find that bees collectively create a scenting-mediated communication network by arranging in a specific spatial distribution where there is a characteristic distance between individuals and directional signaling away from the queen. To better understand such a flow-mediated directional communication strategy, we developed an agent-based model where bee agents obeying simple, local behavioral rules exist in a flow environment in which the chemical signals diffuse and decay. Our model serves as a guide to exploring how physical parameters affect the collective scenting behavior and shows that increased directional bias in scenting leads to a more efficient aggregation process that avoids local equilibrium configurations of isotropic (nondirectional and axisymmetric) communication, such as small bee clusters that persist throughout the simulation. Our results highlight an example of extended classical stigmergy: Rather than depositing static information in the environment, individual bees locally sense and globally manipulate the physical fields of chemical concentration and airflow.

Scent Marks Signal Species, Sex and Reproductive Status in Tamarins (Saguinus spp., Neotropical Primates)

Olfactory communication is an important mediator of social interactions in mammals, thought to provide information about an individual’s identity and current social, reproductive, and health status. In comparison with other taxa such as carnivores and rodents, few studies have examined primate olfactory communication. Tamarins (Callitrichidae) conspicuously deposit odorous secretions, produced by specialized scent glands, in their environment. In this study, we combined behavioral and chemical data on captive cotton-top tamarins, Saguinus oedipus, and bearded emperor tamarins, S. imperator subgrisescens, to examine the role of olfactory communication in the advertisement of species, sex, and reproductive status. We observed no difference in scent-marking behavior between species; however, females marked more frequently than males, and reproductive individuals more than non-reproductive ones. In addition, tamarins predominantly used their anogenital gland when scent-marking, followed by the suprapubic gland. We collected swabs of naturally deposited tamarin anogenital scent marks, and analyzed these samples using headspace gas chromatography-mass spectrometry. Despite a limited sample size, we established differences in tamarin anogenital mark chemical composition between species, sex and reproductive status, and identified 41 compounds. The compounds identified, many of which have been reported in previous work on mammalian semiochemistry, form targets for future bioassay studies to identify semiochemicals. Our non-invasive method for collecting deposited scent marks makes it a promising method for the study of olfactory communication in scent-marking animal species, applicable to field settings and for the study of elusive animals.

Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species

Mammalian chemosignals—or scent marks—are characterized by astounding chemical diversity, reflecting both complex biochemical pathways that produce them and rich information exchange with conspecifics. The microbiome of scent glands was thought to play prominent role in the chemical signal synthesis, with diverse microbiota metabolizing glandular products to produce odorants that may be used as chemosignals. Here, we use gas chromatography–mass spectrometry and metagenomic shotgun sequencing to explore this phenomenon in the anogenital gland secretions (AGS) of the giant panda (Ailuropoda melanoleuca). We find that this gland contains a diverse community of fermentative bacteria with enzymes that support metabolic pathways (e.g., lipid degradation) for the productions of volatile odorants specialized for chemical communication. We found quantitative and qualitative differences in the microbiota between AGS and digestive tract, a finding which was mirrored by differences among chemical compounds that could be used for olfactory communication. Volatile chemical compounds were more diverse and abundant in AGS than fecal samples, and our evidence suggests that metabolic pathways have been specialized for the synthesis of chemosignals for communication. The panda’s microbiome is rich with genes coding for enzymes that participate in the fermentation pathways producing chemical compounds commonly deployed in mammalian chemosignals. These findings illuminate the poorly understood phenomena involved in the role of symbiotic bacteria in the production of chemosignals.

Z4-11Al mediates olfactory attraction and courtship in Drosophila melanogaster

Specific mate communication and recognition underlies reproduction and hence speciation. Mate communication evolves during adaptation to ecological niches and makes use of social signals and habitat cues. Our study provides new insights in Drosophila melanogaster premating olfactory communication, showing that female pheromone Z4-11Al and male pheromone cVA interact with food odour in a sex-specific manner. Furthermore, Z4-11Al, which mediates upwind flight attraction in both sexes, also elicits courtship in experienced males. Twin variants of the olfactory receptor Or69a are co-expressed in the same olfactory sensory neurons, and feed into the same glomerulus in the antennal lobe. Female pheromone Z4-11Al is perceived via Or69aB, while the food odorant (R)-linalool is a main ligand for the other variant, Or69aA. That Z4-11Al mediates courtship in experienced males, not (R)-linalool, is probably due to courtship learning. Behavioural discrimination is reflected by calcium imaging of the antennal lobe, showing distinct glomerular activation patterns by these two compounds. Male sex pheromone cVA is known to affect male and female courtship at close range, but does not elicit upwind flight attraction as a single compound, in to contrast to Z4-11Al. A blend of cVA and the food odour vinegar attracted females, while a blend of female pheromone Z4-11Al and vinegar attracted males instead. Sex-specific upwind flight attraction to blends of food volatiles and male and female pheromone, respectively, adds a new element to Drosophila olfactory premating communication and is an unambiguous paradigm for identifying the behaviourally active components, towards a more complete concept of food-pheromone odour objects.

The effect of social odour context on the amount of time male meadow voles, Microtus pennsylvanicus, self-groom

Communicational behaviours by individuals provide information for not only the intended target(s) of the signal but any non-target individual(s) that may be nearby. For terrestrial mammals a major form of communication and social information is through odours via scent marking and self-grooming. Self-grooming is a ubiquitous behaviour in mammals with the function thought to primarily be centred on personal care. But it has been found in rodents that self-grooming will occur in the presence of social odours thus potentially serving a communicative role. For example, male meadow voles (Microtus pennsylvanicus) self-groom in the presence of a female conspecific odour but not a male conspecific odour. Most studies examining self-grooming as a form of olfactory communication have used single odour donors but in a natural environment individuals will come across complex social odour situations. Therefore, we examined how male meadow voles respond to complex social odours with regards to their self-grooming behaviour. We tested the hypothesis that self-grooming can act as a form of olfactory communication and that male meadow voles will control this behaviour measured by differences in self-grooming rates based on social contexts. Male meadow voles did not show differences in the amount of time spent self-grooming to social odours that contained a female and varying number of rival males (0, 1, 3, or 5) or if the social odour contained an acquainted or novel male. Male meadow voles did self-groom more to a social odour that contained a female and a younger male compared to when the social odour contained a female and older male. Male meadow voles appear to adjust their self-grooming behaviour based on the context of the social information. This may be a strategy that can maximize that individual’s fitness by adjusting how much information is provided to potential rivals and mates.