Friday, August 26, 2016

A mating like no other and why it matters

Note: This blog contains footage of a mating which recently occurred within Talek West. It is used with the permission of the Mara Hyena Project and for scientific purposes only.

If there is one quality about the Mara ecosystem which can be assured, it is the capacity of the park and its inhabitants to remain unpredictable. A few evenings ago, my fellow RA Amy and I were lucky enough to witness our first hyena mating. This occurrence is rare enough in itself, because hyenas often prefer this to be a more private affair. But what made the session especially interesting from an ecological and behavioral perspective was its participants – Decimeter, one of the most highly ranked females in the clan, and Penne, a natal male.

Penne and his brother Ziti have been special cases within our clan. While most males born within the clan (termed “natal males”) begin to disperse as early as age 2, these brothers have been living comfortably in Talek West for more than 6 years and are showing no signs of wanting to leave any time soon. We fixed both of the boys with GPS collars about 3 years ago when they originally began making long scouting forays into nearby territories, a behavior usually indicating imminent dispersal. However, ultimately not one but both brothers have, at least for the immediate time period, decided that Talek West will remain their home. Now, from what we can deduce from our daily observations, the pair spends the majority of their time hanging out with the high ranking females of the recently split off Main DOC group.
ZITI showing off his GPS collar, which will be used to track him if he disperses
For those unfamiliar with dispersal behavior, especially as it occurs in spotted hyenas, it is a phenomenon which is observed in the vast majority of male hyenas (and indeed in many other males of group-living mammals). Dispersal behavior likely evolved both to prevent inbreeding of closely related individuals and to ensure that the male in question breeds in the clan which gives him the best selection of females which are likely to breed with him. Another important factor which the male must consider when scouting for new clans is the resources which he is likely to gain access to, conditional on the hierarchical climate of the females and males (both natal and immigrant) currently within the clan. Ultimately, he will make his choice based upon the best possible combination of these factors and will gain more and more breeding success in his new clan as he gains seniority over new incoming males.

While it cannot be said for certain what prompted Penne and Ziti to make the unconventional choice to stay, there are certain environmental and social conditions which are fairly rare of the Mara and Talek West itself that could minimize the negative aspects of their decision. Firstly, the park itself, in addition to being one of the prime sites of the migration, is home to a large abundance of other wildlife. In these conditions, carnivores like hyenas, who are extremely versatile in behavior and diet and thus a little less susceptible to human disturbance than species like lions, cheetahs, and leopards, flourish, as even the lowest ranking individuals will likely have regular access to food. However, Talek West is not the only clan living in the Mara, and so even if the clan has an extremely favorable atmosphere in terms of access to food, there are dispersal options which likely have similar conditions as well.
PENE shortly before he was collared
One factor which does play a large role in the success of dispersing males verses natal ones is rank. As natal males, our boys Penne and Ziti are automatically ranked higher than every immigrant male who comes to the clan seeking reproductive success. As such, they have priority access to food and mates over all such males. A study conducted by Davidian et al. on eight separate clans in Tanzania found that, although the number of males which did decide to remain within their natal clan to breed was a small minority, said males had significantly more success with medium to highly ranked females. In their study clans, this led to what was considered equal reproductive success for natal and dispersing males, without the natal males having to dispense the time and energy required to find a new clan.

So if one does consider the role of natal rank not only in its propensity to provide the male with access to higher quality females, but also in its ability to give natal males an additional familiarity with the territory and more time to build good relations with prospective mates, why isn’t this considered to be an optimal breeding strategy in clans which have an equal or higher number of breeding females than their neighbors? Something which must be considered is the willingness of breeding females to take as mating partners males which they have grown up with – in fact, the majority of the time this tends not to happen. This behavior was likely selected for concurrently with that of males to disperse and is one of the key factors which aids in the prevention of inbreeding in what is usually a relatively small clan. But what about clans like Talek West, which while still in the process of fissioning has grown to a size of around 200 individuals? On one hand, this may reduce the possible negative effects of inbreeding. While Penne and Decimeter are both a part of Murphy’s sprawling lineage, dominating nearly half of the clan, there are at least 3 degrees of separation in their relatedness (Penne is the grandson of Decimeter’s cousin once removed to be precise). But of course, there is no way our hyenas could know this to be true. Instead one possibility which could be considered is that, with such a large number of individuals in the clan, the number of regular interactions (and possibly the reluctance of the female to mate) is bound to be reduced.
Decimeter is currently the fifth most highly ranked female in the clan.
While it is still overwhelmingly likely that this natal male will get rejected at the end of the day and find better mating success elsewhere, Penne seems to be doing fine remaining where he is for now. Although we have seen him with at least one high ranking female, it may be impossible to know how many willing breeding partners he and his brother will have in this clan. This may yet lead the boys to disperse to a secondary breeding clan with more willing females. Perhaps we may even see others of his kind arise and find the same kind of success in Talek West – only time will tell.

Footage of the mating between PENE and DECM


Davidian, E., Courtiol, A., Wachter, B., Hofer, H., & Ho Ner, O. P. (2016). Why do some males choose to breed at home when most other males disperse? Science Advances, 2(3). doi:10.1126/sciadv.1501236

Monday, August 22, 2016

Goin' Courtin'

Just a few days ago, I had the good luck to see one of our North clan males, Leprechaun, engaged in courting behavior with the matriarch of North clan, Waffles.
A flattering photo of Leprechaun, immigrant male.
An even more flattering photo of Waffles, Clan Matriarch.
Courting is an essential part of a male hyena's mating strategy; because mating is entirely female choice in spotted hyenas, the male has to convince the female that he, in particular, is the best male for her to mate with. Male hyenas have many strategies for this, including affiliative behaviors such as grooming and greeting, following a female around constantly (called "shadowing"), defending a female from the approach of other males, and harassing the object of his affection repeatedly.

What we were lucky enough to see was a courting behavior called "bowing", where the male hyena crosses one front leg over the other to indicate his interest in a female. See for yourself!


Now, just because we saw Leprechaun making overtures to his beloved Waffles, doesn't mean she is even remotely interested in mating with him. As you could see in the video, she was actually relaxing and nursing her cub while Leprechaun was nervously bowing, and hardly paid any attention to him, except for at the end of the video when she was clearly getting annoyed with his presence and aggressed on him.

Unfortunately for Leprechaun, braving this dangerous situation might not even increase his chances at mating with Waffles in the future – she not being sexually receptive at the time of his courting behavior precludes any real chance on Leprechaun's part for siring her next litter of cubs.

Ultimately, the choice of who to mate with is up to Waffles – Leprechaun just needs to be around when she actually wants to mate, not when she is otherwise occupied with cub-rearing!

    East et al. 2003 Sexual conflict in spotted hyenas. Proc R. Soc. Lond.
    Szykman et al. 2001 Association patterns among male and female spotted hyenas reflect male mate choice. Behav Ecol Sociobiol.50: 231-238.

Monday, August 15, 2016

Self-control matters in spotted hyenas

Hey, it's Lily again. I'm a graduate student out in the field right now collecting cognitive data with the hyenas. One of the cognitive tasks I’m giving hyenas tests self-control, which is also known as “inhibitory control” in many scientific studies. Inhibitory control is the ability to resist a prepotent motor impulse in circumstances that demand restraint. In humans, the “marshmallow test” is a famous self-control test given to small kids. Children are presented with a marshmallow and told that if they can wait fifteen minutes without eating the marshmallow they’ll be rewarded with a second marshmallow. Inhibiting the impulse to eat the marshmallow right in front of them is extremely difficult for many kids and how well kids do on this task is highly predictive of success in life as adults.
The Marshmallow Test 
Inhibitory control is important for other cognitive abilities because it’s thought to be a precursor to more complex thought. Before thinking about how to solve a problem, one must be able to take a step back to assess a situation, i.e. “stop and think”. 

I’m testing inhibitory control in spotted hyenas using a tube task. It’s a standard task for testing inhibitory control in animals and is part of a family of “detour tasks”. Detour tasks test inhibitory control by requiring an animal to initially move away from a food reward before moving towards it to retrieve it. 
An example of a detour task conducted with dogs.
This is often done by placing a barrier, like a fence, in front of a clearly visible food reward. In order to get the food, the animal must walk around through a gap in the fence, which requires moving away from the desired food reward. This can be really difficult for many animals who want to run straight towards the food!

A juvenile spotted hyena interacting with the tube task.
The tube task uses a transparent cylinder the rests horizontally on the ground with both ends open. The animal is presented with the tube and they must reach inside either end of the tube without bumping into the side of the tube. Prior to test trials with the clear tube, they are given familiarization trials with a solid tube so that they learn where the openings on the tube are.
An adult female approaches the familiarization tube.
Spotted hyenas are so proving themselves to be quite good at this task, but they occasionally have lapses in their self-control!

SRG fails the tube task.

SRG passes the tube task.

In animals, inhibitory control is related to brain size, dietary breadth, and the degree of fission fusion dynamics. (MacLean et al. 2014; Amici et al. 2008). Amy Fontaine wrote about fission fusion dynamics (FFD) in an earlier blog post here. Animal societies with a high degree of FFD are those like chimpanzee society. Individuals live in large social groups, but most of the time the entire social group does not live together. Instead, they break up into small subgroups of just a few animals and only come together in large groups for specific events. This means that individuals in a social group sometimes go days, weeks, or even months, without seeing some of their group mates. This kind of social living is thought to be cognitively challenging because individuals must remember the identities and social ranks of all their group mates even though they don’t see them that often.

For hyenas, living in a high FFD society is adaptive because it means they can split up to look for food but join together when they need to fight off lions or other hyena clans to defend their territory (Smith et al. 2008). 
Hyenas from Happy Zebra Clan go on a border patrol.
Observing hyenas in the field it’s easy to see that they have great inhibitory control. I’ve seen hyenas patiently wait for hours around a mother giraffe who’d had a still-born calf. They all had the inhibitory control to not mess with the mom, an adult giraffe has a very powerful kick, and instead went to sleep about 30m away from her to wait for her to abandon the still-born calf. In addition, hyenas will wait patiently around a carcass that lions have control of. An adult male lion can kill a hyena with a single swipe of the paw and hyenas have to have the inhibitory control to know just when they can go in and steal food without getting hurt. Out in the Mara, a hyena without inhibitory control will get killed!
A hyena waits for a mother giraffe to leave the still born calf at her feet. 
In addition, spotted hyenas require a lot of inhibitory control in the social domain. Lower ranking hyenas have to inhibit all aggression towards higher rankers, especially when food is present. I’m especially interested in inhibitory control in male hyenas. When hyenas are born, they obtain a social rank directly below their mothers in the hierarchy. Some male hyenas are born as high rankers and some are born as low rankers. However, when male hyenas hit sexual maturity they leave to join a new clan in search of mating opportunities. When a male hyena joins a new clan, he joins at the very bottom of the hierarchy. In their new clans, male hyenas must possess an extraordinary degree of inhibitory control and inhibit all aggression around their new clan mates. Because male hyenas are “destined” to become extremely low ranking when they’re adults and clearly learn to inhibit all social aggression around females and other hyenas in their new clans I think they’ll have much better self-control on the tube task.
A male hyena shows submission by going ears back to an aggressive female. 
The interesting part is, I will also be able to test a prediction of the social brain hypothesis. The social brain hypothesis predicts that big brains are a result of the cognitive demands of living in complex social groups. So far, the social brain hypothesis makes strong predictions in primates and complex sociality does predict complex social cognitive skills, but it’s unclear if social pressures select for cognitive skills outside the social realm. I.e. it’s not clear that complex sociality predicts things like tool-use or spatial navigation. So, just because male hyenas have great inhibitory control in the social realm, it’s not totally clear that they will have great inhibitory control on a physical task like the tube task.  If they do, it means that social inhibitory control also makes male hyenas better at physical inhibitory control!
A hyena plays with the opaque tube.
Amici, F., Aureli, F. & Call, J., 2008. Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates. Current biology : CB, 18(18), pp.1415–9.
MacLean, E.L. et al., 2014. The evolution of self-control. Proceedings of the National Academy of Sciences of the United States of America, 111(20), pp.E2140–8.
Smith, J.E. et al., 2008. Social and ecological determinants of fission–fusion dynamics in the spotted hyaena. Animal Behaviour, 76(3), pp.619–636.

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