Smells like hyena spirit

hyenamicrobesymbiosis

Have you ever found yourself walking through the African savannah and wondering what the odorous light brown goop found on various strands of grass is? Me neither, but that’s probably just because I’ve never been in the African savannah, let alone traveled to sub-Saharan Africa. If I had had that opportunity, however, I may have observed (or smelled) this rather-nasty-sounding substance, referred to by scientists as “paste”. This paste, quite different from the tooth, adhesive, and caviar varieties, is the foul-smelling calling-card of the gregarious, savannah-dwelling hyenas. Excreted from a specialized scent gland under hyenas’ tails and rubbed onto grass stalks throughout the hyena’s habitat, paste is a vehicle for chemical communication between one hyena and another. This behavior (referred to as “pasting”) is a form of scent marking, a chemical signaling behavior widely used by mammalian species to establish territory or communicate complex information such as identity, sex, reproductive status, social status, kinship, and/or group membership. Each individual hyena’s paste has a unique chemical signature, a complex mixture of volatile fatty acids, esters, hydrocarbons, alcohols, and/or aldehydes, whose specific chemical composition and varying concentrations of these components can communicate identity. Indeed, the individual chemicals present and concentrations in wild hyena paste have been shown to vary with hyena identity, group membership, sex, and reproductive state. Although the paste overall exudes a fermenting mulch-like smell (to us, at least), the slight variations in the individual odors appear to have differential effects on hyena behavior, possibly influencing the complex social structure of these species.

This convoluted chemical signature of identity, as well as the apparent ability of hyenas to interpret and differentiate the presence and concentration of certain chemicals, is in itself an amazing chemical ecology story. In my opinion, however, this chemical communication narrative has become even more fascinating as scientists have begun to investigate the molecular source of the pungent “chemical bouquets” found in hyena paste. Like many mammalian specialized scent glands, the glands found underneath the hyenas’ tails are warm, moist, and nutrient-rich- basically, ideal environments for prolific microbial growth. Although it historically has been difficult to identity and characterize the symbiotic microbial communities that reside in mammalian scent glands (the vast majority of microbes found on the planet cannot be cultured in typical lab settings!), scientists have long suspected that these bacterial residents may play a role in generating the social odors of their host. This hypothesis, formally called the “fermentation hypothesis,” posits that as the microbial symbionts metabolize the nutrient-rich substrates found in the scent glands, they generate odorous metabolites that can be hijacked by a mammalian host for communication. Variations in the microbial community found in hyena scent glands (i.e. the presence and abundance of certain species) may thus correlate with variations in metabolite production, creating a unique paste scent for the host. If this hypothesis is true, when hyenas are spreading their paste throughout the savannah, they are actually depositing part of a unique scent-gland microbial community and relying on these microscopic organisms and their metabolism to communicate their identity.

Recently, this hypothesis was explored for the first time in wild hyena populations by a biologist at Michigan State, Kevin Theis. Prof. Theis and co-workers traveled to Kenya’s Masai Mara National Reserve to track different spotted and striped hyena populations and occasionally dart and tranquilize individuals from these communities. While the hyenas were peacefully sleeping, the scientists used a scapel to remove the paste from their posterior scent glands. They then flash froze the paste samples and sent them back to the US for analysis. Taking advantage of modern DNA sequencing technology that can be used to identify bacterial strains by the sequence of a species-specific characteristic gene (termed 16s sequencing), Theis and co-workers were able to identity the presence and abundance of certain bacterial strains in each individual hyena’s paste. Additionally, they were able to use standard analytical methods to characterize and quantify the chemicals odors produced in each individual paste. Their results, published in PNAS, indicated that microbial communities present in paste are dominated by fermentative anaerobic species (such as Clostridial species) and that the bacterial communities, as well as the odors produced, differed between the two species of hyenas, as well as signaled the identity of the hyena as a female or male, and if the females were pregnant or lactating.

Although the data collected by Theis and co-workers strongly suggested that hyenas use bacteria to mediate social scent-based communication, it does not provide conclusive proof and many questions inevitably remain. What genetic or biochemical links can be established between certain microbial species present in the paste and the odors produced? Can hyena communication systems be disrupted by antibiotics? What correlations exist between these microbes and metabolites and hyena behavior? Do specific microbes or the molecules they produce trigger specific behaviors?  

Perhaps the most intriguing question, however, is: how can these bacterial communities and the metabolites they produce actually communicate any information about the hyena they inhabit? It may not be as far-fetched as it may seem. Many factors are known to play a role in establishing and modifying bacterial communities in an animal host- including genotype, physiology, diet, social relationships, and the environment. The microbes that live on and within a young mammal are typically derived from the mother’s birth canal, as well as its environmental surroundings. One could thus imagine a correlation between microbial communities and familial relations, as well as the sharing of bacteria between hyenas that live together as a clan. Additionally, as the host ages, changes in physiology could also influence the structure of its microbial community- for example, the differences in physiology and hormonal levels between a pregnant and a non-pregnant female may change the bacterial environment, favoring the growth of one type of bacteria over another. Together through these sorts of correlations/hypotheses, one may begin to appreciate how bacterial community structure may be indeed be predictive of host identity, and that perhaps its not surprising that bacterial-derived odors may communicate this type of information.

Unfortunately, further exploration of the role bacteria play in hyena scent communication may be limited, considering the test subjects are large, wild (and scary?) carnivores. Fortunately, numerous other organisms are hypothesized to rely on bacteria for chemical communication, and scientists- biologists, microbiologists, and chemists alike- are very interested in studying the characteristics and mechanisms of these types of animal-microbe interactions. Hopefully the next few decades of research will be fruitful in expanding our understanding of (and appreciation for!) microbial-mediated animal communication. In the meantime, however, we’ll just try to wrap our heads around the fact that these teeny, tiny, unseen microbial species are microscopic agents influencing the complex social behavior of charismatic megafauna like the hyena! 

- KLS