Animals are almost completely covered by bacteria, inside and out. Most of these microbes help out by breaking down food and defending against harmful invaders—all in return for room and board. New research finds that these communities of microbes, called the microbiome, may also affect an animal’s behavior.
Kevin Theis, an animal-microbial ecologist at Michigan State University, studies how the microbiome enhances communication in a surprisingly social creature: spotted hyenas. The animals make a compound called “paste” inside their warm, moist scent pouches that gives each hyena a characteristic smell. They deposit that paste around their territories by rubbing their pouch, located just above the rectum, against stalks of grass to leave behind small smears.
Theis and his colleagues sequenced the DNA from bacterial communities living in the scent pouches of two hyena species. They found that the communities in highly social spotted hyenas are twice as complex as those living in striped hyenas, which live mostly solitary lives. These newly discovered bacterial communities—and their scents—vary depending on the sex of the hyena, and whether a female is pregnant or lactating.
As Theis reported in a 2013 article in the Proceedings of the National Academy of Sciences, these findings support the “fermentation hypothesis for chemical communication.” This idea posits that animals pick up information from each other using the odors created by bacteria that ferment bodily secretions. The scents can say whether an animal is one of the herd and if it is available for mating.
Theis spoke about his work at the February 2014 meeting of the American Association for the Advancement of Science in Chicago. Afterward, he shared the appeal of hyena paste with SciCom’s Patricia Waldron.
How did you first become interested in hyenas?
I wanted to study behavioral ecology, and there was a certain allure to carnivores. My original interest was grey wolves. I had read “The Wolf” by David Mech and became fascinated that there were people whose career it was to go out in the wild and just learn everything. But it became clear that studying wolves would be listening to howls and playing with scat, so fortunately my undergrad thesis advisor had known Kay Holekamp [a hyena behavioral ecologist at Michigan State] and suggested I look into hyenas—an incredibly fortuitous turn of events because their social structure is just so remarkable.
When did you begin studying scent communication?
I had gone to grad school to study vocal communication. But I went into the field and I saw them engaging in this scent-marking behavior. I asked Kay, “What are they doing?” She said, “We don’t really know. No one has studied it, but I have a freezer full of paste samples I’ve been waiting for someone to study.” They did it so often and they did it in so many social contexts. It was too much to pass up.
You lived in Kenya for over a year for your fieldwork. Did you interact with the local people?
Hyena researchers have friends at the local tourist lodges and in Talek town and its surrounding villages. They regularly visit these friends for discussion over chai or a beer. The visits I most enjoyed were from female elders, as they typically had a great sense of humor. Also, all hyena researchers give informal talks to tourist groups and some have contributed to curricula in the local school.
How did you study the spotted hyenas in the Masai Mara National Reserve?
We have radio collars on some of the primary members of the clans so we can locate them daily, at dawn and dusk. I did quite a bit of night work because they are primarily nocturnal. I would switch on my night vision equipment and sit and watch them until two in the morning.
What was it like working at night?
I had lots of great interactions with hippos and elephants surrounding my car while trying to do scent discrimination experiments. Being out at night was a remarkable experience. One of the things that researchers pride themselves on is seeing an aardvark, which only comes out at night. I never did, and that’s bothered me to this day.
What is so interesting about spotted hyena family structure?
In spotted hyenas there are multiple overlapping generations of females. The highest ranking female and all her kids will be in the alpha position. Then her sisters and their offspring will maintain positions just below that, and so on, until you get to the lowest ranking members of the clan.
Your colleague Aaron Wagner sampled the microbiome from striped hyenas. How are they different?
Striped hyenas all disperse, so it’s largely going to be an adult female in a territory that just has one or two males. Even if they share home ranges, they’re functionally solitary.
Aaron set up leg holds or box-traps. You can’t sit and watch them like you do spotted hyenas. They’re habituated to us and we watch their life unfold like a soap opera. Striped hyenas are solitary, they’re moving, and they’re much more difficult to observe.
"If I were a bacterium, particularly a fermenter, I couldn’t think of a better spa than a hyena scent pouch."
When dogs sniff each other, is that equivalent to when hyenas smell paste markings?
Very similar. Whether they’re getting the same kinds of information as hyenas, I’m not sure. But odor cues are providing information about the animal.
Why do spotted hyenas paste?
Territoriality. Males are using it to advertise social status and females to facilitate social cohesion.
And pasting is enough to keep other hyenas out of their group?
It’s not a fence, so males come and go pretty freely. They come in and they’re seeing if the clan’s going to be a good fit. You can get transient females coming through, but you won’t get a big spillover. Paste is probably providing them information about the ability of that other clan to defend that territory, but it’s not stopping them from going back and forth.
What does paste smell like?
To me, it smells like when you do landscaping in the summer and it rains—that odor of mulch. Other people say I’m crazy and that they smell burnt soap. I don’t know what burnt soap smells like, but I’ve heard it characterized as that. Some people actually can’t smell paste at all.
How do you collect the paste?
We do it in two different ways. We anesthetize the animal and take all sorts of [body measurements] and collect blood for DNA work. We take a scalpel handle, sterilize it and scoop it right out [of the scent pouch]. There’s actually quite a bit in there. The other way we collect it, for a non-invasive approach, is the grass stalks. Obviously then you have the potential issue of multiple animals having pasted in that spot. You have to be careful, but we can get more samples that way.
Do spotted hyenas use chemical cues from scent pouches to choose mates?
Females seem to make mate choice decisions based upon how long a male has been in the clan. I think pasting allows males to get credit for time served. You’ll see them show up to a communal den and it’s like they do a run through. If they put paste in places where females are going to encounter it, the females are going to recognize that they’ve been around, and that could facilitate being chosen.
In your talk, you mentioned that lactating and pregnant females have different scent profiles. Do they have different behavior too?
When females are pregnant, they paste at much higher rates than when they’re lactating. I’ve hypothesized that they’re getting the clan ready for their cub to come into the world. I suspect it may be a way to reintroduce themselves into the immediacy of the clan before their cubs come in. Sometimes females will take extended leaves of absence from the clan. When they come back, their pasting rates are markedly higher than before they left, so there too it seems like pasting could be reintroduction.
What factors within the hyena scent pouch might affect the composition of the microbiome?
I have a hypothesis that it’s their endocrine profile. Pregnant females have very different levels of circulating hormones than do lactating females. We know that in humans, you have interactions in sebaceous glands between hormones and skin bacteria. I’d be incredibly surprised if a similar sort of thing weren’t going on in the hyena scent pouch.
What do the bacteria get out of the deal?
A place to live! If I were a bacterium, particularly a fermenter, I couldn’t think of a better spa than a hyena scent pouch.
Many bacterial DNA sequences that you found in scent pouches were previously unknown, but the microbes likely need an oxygen-free environment. How do these “anaerobes” survive on a grass stalk until they find their way into a scent pouch?
Spores.
Oh. Of course.
One of the problems with these novel bacteria is I don’t know their life histories. Some are spore-formers [bacteria that can transform into a dormant seed-like state], so that could be a way to get cross-infection. You know this, having done your master's degree in micro: even if it’s an anaerobe, it doesn’t mean it can’t survive an oxygen pulse.
What’s really cool are European badgers. They engage in this behavior called allomarking, where they literally extrude their scent pouches and press them together [does fist bump to simulate allomarking]. Now there, you don’t have to worry about [oxygen].
It seems like research into chemical communication started in the 1970s, but hasn’t taken off until recently. Why has this field taken so long to develop?
As molecular fingerprinting techniques came along, I think the pace picked up a little bit. Now I think you’re going to see a lot more, because you have bench-top [DNA sequencing] machines. Anyone can do it now.
Do you expect that other animals use bacterial odors to send chemical signals?
I really do. It can be such a nuanced mechanism. Your microbes can be such a reflection of you that their metabolites can convey that information to anyone that’s interested.
Do humans use microbial odors to communicate?
I’m not going to go so far to say that it’s signaling. But humans have the capacity to identify odor cues that have to do with underlying [genes], and it’s entirely probable that bacteria are playing a role. I’ve often wondered why people aren’t doing more experimental work with microbes in human odor cues.
Do you think about scents all the time?
I not only think about odor constantly, I think about microbes constantly. I wouldn’t say it’s ruined anything for me, but I spend a significant portion of my day thinking about odor and what microbes are doing that may not be immediately evident to us.
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© 2014 Patricia Waldron
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