What do geladas and humans have in common? Apparently, vocal patterns.

T. gelada. Photo: Ron Waddington

They live in very large groups called herds, they primarily graze on terrestrial vegetation, and they roam on large open plains. In more than a few ways, geladas (Theropithecus gelada) are similar to cows. Geladas are more vocal than cows though. They have a diverse range of vocalizations for various behaviors and situations, such as contact, showing submission, aggression, and others (Kawai, 1979; Aich et al., 1990).  The diversity and complex communication exhibited by geladas is one of the reasons this is a very interesting primate species to study.

A new study on their vocal sequences shows that this species of Old World Monkey follows patterns that are similar to humans. As far back as the late eighties, Richman (1987) suggested the geladas use melody and rhythm in ways similar to humans. Now, Gustison and colleagues have shown that the longer the sequence of sounds is that a gelada makes, the shorter the sounds within that long sequence. This is the same pattern observed in humans and is called Menzerath's law. The longer our sentences, the shorter the words tend to be in those sentences.

The authors studied fifty-seven male geladas in the wild and recorded and analyzed over 1000 vocal sequences. In addition to discovering that longer sequences are made up of shorter calls, Gustison and colleagues report that long sequences start with short calls and short sequences start with long calls. Thus, the start of the sequence is an indicator of its overall length. Longer sequences also have faster tempos. Gustison and colleagues state this might be to reduce the possibility of one gelada being "talked over" by another. You can understand how this might be a problem in a chatty species that lives on open plains. If you have a lot to say, you better say it quickly.

Geladas grazing. Photo Alastair Rae

Interestingly, there was no negative relationship between the position of a call and its duration (calls later in the sequence were not shorter). Yet, the proportion of grunts where the gelada was exhaling decreased in longer sequences and the proportion of grunts where the individual inhaled increased. The authors believe this pattern is due to the fact that individuals make grunts with both inhalations and exhalations on the same breath as the sequence lengthens. Once geladas have more than 15 calls per sequence, the majority of their calls have both inhale and exhale grunts and the proportion of inhale and exhale grunts hardly varies.  Thus, respiration and energy demands may constrain gelada vocalizations, and be partially the reason for conforming with Menzerath's law.

This is the first time Menzerath's law has been studied in non-humans. Thus, other animals with expansive vocal repertories, such as songbirds, may also exhibit this law. It is hard to draw conclusions about the evolution of communication in non-human primates and our human ancestors without knowing if Menzerath's law holds true for species that are further separated from humans. For now, we know humans are not unique in adhering to Menzerath's law.  It is possible that this pattern existed before meaningful combinations of vocalizations had evolved. Tests in other species will only serve to improve our understanding of sequences, vocal patterns, and the evolution of language and communication in general.



Links of potential interest:
Menzerath's Law
IUCN page on geladas
YouTube video on gelada chatter

Works cited:

Aich, H., Moos-Heilen, R., & Zimmermann, E. (1990). Vocalizations of adult gelada baboons (Theropithecus gelada): acoustic structure and behavioural context. Folia primatologica, 55(3-4), 109-132.
Kawai, M. (1979). Auditory communication and social relations. Ecological and Sociological Studies of Gelada Baboons, 219-241.
Gustison, M., Semple, S., Ferrer-I-Rancho, R, Bergmann, T. (in press). Gelada vocal sequences follow Menzerath’s linguistic law. PNAS. www.pnas.org/cgi/doi/10.1073/pnas.1522072113 
Richman, B. (1987). Rhythm and melody in gelada vocal exchanges. Primates, 28(2), 199-223.

New research on vocalizations, grooming, and social bonds

Lemur catta Photo: author

Both grooming and vocalizing are linked to social bonds and relationships. Increases in the vocal repertoire of primates is correlated with group size and amount of time spent grooming (McComb and Semple, 2005). Previous research has shown that pairs of baboons (Papio cynocephalus) spend more time grooming one another (allo-grooming) and allo-groom more frequently if they are bonded socially (Silk et al., 2006). Dunbar first suggested that vocalizations may serve to act as a way of socially bonding when larger group sizes make grooming every member more difficult (1993; 2003; 2004).

A study published this December provides further insight into the reasons why small talk may have evolved and how it relates to social relationships. Studying ring-tailed lemurs (Lemur catta), Kulahci and colleagues (2015) examined vocalizations and grooming.  Four troops of free-ranging and semi-freeranging lemurs at the Duke Lemur Center and on St. Catherine's Island were studied. Vocalization and grooming network outdegrees were calculated to determine who each individual initiated vocalizations and grooming towards. The grooming network outdegree was simply the number of individuals the individual in question groomed. The vocalization network outdegree was   the number of individuals that the individual in question produced a vocal response towards upon hearing a call.

Kulahci and colleagues (2015) found that ring-tailed lemurs were more selective in who they vocalized to than who they chose to groom: as troop size increased, lemurs groomed more individuals but they did not vocalize directly towards more individuals. Regardless of troop size, vocalization network outdegrees were lower than grooming network outdegrees, showing that lemur are picky about who they vocalize to but less so about who they groom. Individuals responded to the vocalizations of lemurs they groomed more frequently than they did lemurs they groomed less often.

When audio playbacks were used, the same selectivity in vocalization responses was displayed. Thus, this selectivity in vocalizations is not due to olfactory or visual cues.

While this study agrees with previous work highlighting the connection between grooming and vocalizations, it does not align with Dunbar's hypothesis (1993; 2003; 2004) that vocalizations allow an individual to maintain more social bonds than grooming would. Whereas we would have expected to see vocalizations increase with group size, the opposite was true for this study. Rather than vocalize with more troop members as group size increases, L. catta selectively vocalize and groom all members. Thus, vocalizations may be a better indicator of social bonds than grooming, at least in L. catta.

Links of possible interest:
 Social grooming in primates
How the size of the neocortex and the size of grooming clusters relate
Derived vocal complexity of geladas


Sources:

Dunbar, R. I. (1993). Coevolution of neocortical size, group size and language in humans. Behavioral and brain sciences, 16(04), 681-694.

Dunbar, R. I. (2003). The social brain: mind, language, and society in evolutionary perspective. Annual Review of Anthropology, 163-181.

 

Dunbar, R. I. (2004). Gossip in evolutionary perspective. Review of general psychology, 8(2), 100.

 

Kulahci, I. G., Rubenstein, D. I., & Ghazanfar, A. A. (2015). Lemurs groom-at-a-distance through vocal networks. Animal Behaviour, 110, 179-186.

 

McComb, K., & Semple, S. (2005). Coevolution of vocal communication and sociality in primates. Biology Letters, 1(4), 381-385.

 

Silk, J. B., Altmann, J., & Alberts, S. C. (2006). Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behavioral Ecology and Sociobiology, 61(2), 183-195.

 

 

Olive baboons can be democratic when it comes to troop movement

Olive baboons (Papio anubis) live in a world where social rank matters. They live in troops that can have over one hundred individuals, with females remaining in their natal group and males dispersing. Males are dominant over females but females have a strict linear dominance hierarchy, meaning who your mother is matters. A lot. Related females groom each other and have each others backs in agonistic meetings.

Photo credit: Nevit Dilmen

A new study out in Science by Strandburg-Peshkin and colleagues shows that, much to everyone's surprise, olive baboons are democratic when it comes to troop movement. Yep, these primates, which can be known for their aggression (just look at those canines), don't bully when it comes to choosing where to go.

What we'd expect in a primate with such a strict social system is that the group would go where dominant individuals want to go. Those lower on the social totem pole aren't going to act against a more dominant individual's decision nor are they going to attempt to make these decisions themselves. However, using GPS technology, researchers found that the troop tends to go where multiple initiators want to go and individuals who move in a directed manner are more likely to be followed.

When two groups within a troop are moving in different directions, the larger group is more likely to win, and this likelihood grows as the difference in size between the two groups of initiators grows. The authors failed to clarify if, of those decisions with multiple initiators, the number of dominant individuals within groups of initiators made a difference. I'd like to know if five low-ranking individuals could top two high-ranking individuals, when determining which direction to go. Does social rank really have no effect? I'm not sure I'm entirely convinced that it doesn't, but I also don't study baboons.

Now, this study was conducted by studying 33 out of 46 members of one baboon troop over nine days, so it'd be interesting to see if results differ in other troops, in troops of differing sizes, or during different times of the year (for example, when food resources are low). It'd also be interesting to see if this finding holds true for other species of baboons. For example, previous research has shown chacma baboons (Papio ursinus) do pay attention to social relations when deciding which patches of food to target (Marshall et al., 2012).

Food for thought:
Strandburg-Peshkin and colleagues didn't find any differences based on sex when it came to an individual initiating troop movement. Why is this surprising?
Why might this system (in which the troop is democratic in deciding where to go) be adaptive to baboons? When might it not be?

Links of potential interest:
Olive baboon behavior and social organization
Chacma baboon study


Literature cited:
Ariana Strandburg-Peshkin, Damien R. Farine, Iain D. Couzin, and Margaret C. Crofoot. Shared decision-making drives collective movement in wild baboons. Science, 19 June 2015 DOI: 10.1126/science.aaa5099

Harry H. Marshall, Alecia J. Carter, Tim Coulson, J. Marcus Rowcliffe, Guy Cowlishaw. Exploring Foraging Decisions in a Social Primate Using Discrete-Choice Models. The American Naturalist, 2012; 180 (4): 481 DOI: 10.1086/667587

Rank affects a female's likelihood to seek out "friendships"

Photo: Chris Allen

Chimpanzees (Pan troglodytes) are social creatures, living in a fission-fusion society, meaning one large group often breaks into smaller ones to form feeding parties. In the chimp world, males outrank females and there is a strict linear hierarchy to male relationships (Goldberg & Wrangham 1997). Whereas males can remain in their natal group, females migrate around the time when they reach adolescence (years 9-14) (Nishida et al. 2003). Thus, females eventually need to make new friends, whereas males have the benefit of life-long buddies. In most chimpanzee populations, females spend a lot of time by themselves (Williams, Liu, and Pusey, 2002). At Gombe, the famous site where Jane Goodall first went to the wild and studied chimpanzees, females spend the majority of their time alone or with a few other family members (Wrangham and Smuts, 1980; Goodall, 1986).

Gombe National Park in Tanzania, Google Earth

A study due to be published next month in the journal Animal Behaviour reports new insights into the "friendships" of female chimpanzees. (Friendship may very well be too strong of a word. Acquaintance or association is likely more accurate.) Foerster and colleagues used thirty-eight years of data from Gombe National Park and show that female chimpanzees aren't just bonding randomly with each other. Unsurprisingly, mothers, daughters, and sisters form the strongest bonds. However, among unrelated females, those of a low rank were more likely to seek out other females than were mid or high-ranking females. They also sought out other low-ranking females. 

There are multiple reasons low-ranking females might seek out others of the same rank. As Foerster and colleagues suggest, perhaps having an additional low-ranking pal makes competing for food easier or perhaps they seek others to dissuade higher-ranking members from bullying. The reason for their increased likelihood to seek out other female friends remains unknown at the time. It would be interesting to know how long these partnerships last. If they're temporary, why? What circumstances or events cause the end of the partnership?

 Finally, the presence or absence of offspring affects the likelihood a female will seek out other unrelated females. Females with young female offspring associate with other females less than expected, but females with young male offspring seek each other out. This may because it is especially important for males to interact socially with each other and bond, given that those bonds have the potential to last a life time. The same cannot be said for young female chimpanzees because they will eventually leave and find a new troop. Thus, it apparently is worth forming relationships with other young females within the troop.

Food for thought: What are the benefits and disadvantages to spending time with others (if you're a chimpanzee)?
How might this study differ if the study species had been bonobos? Remember, they have a very different social system!

Links of interest:
ScienceDaily article
Chimpanzee social systems
Chimps create traditions video clip
IUCN Redlist page on chimpanzees
Female chimps more likely to use tools
How human are chimps?


References:
Foerster, S, McLellan, K, Schroepfer-Walker, K, Murray, CM, Krupenye, C, Gilby IC, Pusey, AE. Social bonds in the dispersing sex: partner preferences among adult female chimpanzees. Animal Behaviour, 2015; 105: 139 DOI: 10.1016/j.anbehav.2015.04.012
Goldberg TL, Wrangham RW. 1997. Genetic correlates of social behavior in wild chimpanzees: evidence from mitochondrial DNA. Anim Beh 54: 559-70. 
Goodall J. 1986. The chimpanzees of Gombe. Cambridge (MS): Belknap Pr.
Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, et al. 2003. Demography, female life history and reproductive profiles among the chimpanzees of Mahale. Am J Prim 59(3): 99-121. 
Williams, J. M., Liu, H. & Pusey, A. E. 2002. Costs and benefits of grouping in female chimpanzees at Gombe. In: Behavioral Diversity in Pan. (Ed. by Boesch, C., Hohmann, G., and Marchant, L. F.) pp. 192-203. Cambridge: Cambridge University Press.
Wrangham, R. and Smuts, B.B. (1980). Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. Journal of Reproduction and Fertility. Supplement, 28, 13-31.

Are the famous, sex-loving bonobos really more peaceful than their chimpanzee relatives?

Juvenile bonobo eating

Bonobos (Pan paniscus) are often referred to as the peaceful apes or the "make love, not war" apes. Previously known as the pygmy chimpanzee, they're thought of as more gentle and peaceful than their closely related cousins, the chimpanzee (Pan troglodytes). These two species are very closely related: 99.6% of their genome is the same.  Many people are aware that chimpanzees hunt other primates. You may even have heard that they will go to war against other chimps, brutally killing members of their own species, wiping out another group of chimpanzees.  With 99.6% of their DNA identical to chimpanzees, do bonobos really deserve this wholesome image?

Bonobos are only found in the Democratic Republic of Congo. They're smaller in body statue than chimpanzees but otherwise they look very much alike. In chimpanzee social systems, the males are dominant over the females. In bonobo groups, its the females who are dominant over males. Females remain in their natal unit and develop strong bonds with other females. Bonobos also play more as adults, engage in sexual activity more, and display less severe aggression than chimpanzees. So far, it looks like bonobos are living up to their reputation as the more peaceful primate.

As we learn more and more about bonobos, at least one of our original ideas about them has been proven wrong. Originally, only chimps were thought to hunt and eat other primates, but this isn't true. Surbeck and Hohmann (2008) published the first account of wild bonobos hunting other monkeys. Both males and females were active in the hunts and red colobus monkeys, black mangabeys, and other primate species were on the dinner menu for bonobos.  Seems like we've busted that myth.

Bonobos sharing food

However, a study compiling over fifty years worth of data on chimpanzees and bonobos seems to suggest that there is quite a difference. Studying 18 communities of chimps versus 4 communities of bonobos, scientists reported 152 killings by chimpanzees compared to just one killing by bonobos (Wilson et al., 2014). It is thought that differences in the brain between these two great apes may be the underlying cause behind the increased violence and aggression seen in chimpanzees. The brain of a bonobo seems to be better adapted to impulse control, perceiving stress in others. Rilling and colleagues (2012)  state that their neurology "...allows them to more strongly represent distress of both self and others compared with chimpanzees. This translates into greater empathy, as well as reduced aggression." The Rilling article is a great read, as it includes not only their findings but also a thorough overview of the behavioral differences between chimpanzees and bonobos.

To summarize, while there may not be much separating these two species in terms of their DNA, how their DNA is expressed does appear quite different. At first, scientists wondered if we simply had less data available to us on bonobos, and that lack of data meant we were missing behaviors in bonobos that are seen in chimps. (The chimpanzee population is far larger than the bonobo population.) As we study them more and more, chimpanzees come out on top in terms of aggressive behaviors.  It's important to remember through that all of these aggressive behaviors don't make up the majority of a chimpanzee's day. It's quite the opposite. Social behaviors make up a small amount of any primate's day. Feeding and resting take top priority. That said, I think the conclusion that bonobos are more peaceful than chimpanzees stands for now.


Food for thought: I think it's most surprising that bonobos will share first with strangers before they share with friends or associate bonobos (Tan and Hare, 2013). This isn't something we see with chimpanzees (and arguably something we don't see in all humans). Why would a bonobo share with a stranger first? How is this an adaptive behavior?

Check out this incredible BBC video explaining the hunting tactics of chimpanzees. (Yes, they really do have tactics.)

Read NOVA's interview with the well-known primatologist, Frans de Waal, about studying bonobos.

Journal articles referenced:
Surbeck, M., & Hohmann, G. (2008). Primate hunting by bonobos at LuiKotale, salonga national park. Current Biology, 18(19), R906-R907. doi:10.1016/j.cub.2008.08.040
Wilson, M. L., Boesch, C., Fruth, B., Furuichi, T., Gilby, I. C., Hashimoto, C., . . . Wrangham, R. W. (2014). Lethal aggression in pan is better explained by adaptive strategies than human impacts. Nature, 513(7518), 414. 
Rilling, J. K., Scholz, J., Preuss, T. M., Glasser, M. F., Errangi, B. K., & Behrens, T. E. (2012). Differences between chimpanzees and bonobos in neural systems supporting social cognition. Social Cognitive and Affective Neuroscience, 7(4), 369-379. doi:10.1093/scan/nsr017
Tan J, Hare B. Bonobos Share with Strangers. PLOS ONE, 2013; 8 (1): e51922 DOI: 10.1371/journal.pone.0051922

Living with others

I spend my days alternating between three troops of Verreaux’s sifakas. Two of my troops contain six individuals and one troop contains seven. Verreaux’s sifaka group size ranges from one individual to up to ten members. Here in Berenty, I’ve seen quite a few groups with six or seven individuals. Although, group size is much smaller in the spiny forest, which is very dry and where food is potentially limited.

Resting midday

Most species of primates live in social groups. While some members may live on their own for some time after they disperse from their natal group to seek new mating opportunities, many primates will spend the majority of their lives living with others. Living in a group has its advantages and disadvantages. Living in a larger group means better protection against predators, such as snakes, birds of prey, and cats. An individual may feed and feel a little safer, knowing that multiple eyes and ears are on the lookout. Larger groups are also better able to defend resources, such as a valuable fruiting or flowering tree. Primates have competition from members of their own species and members of other species, and a larger group size may mean the difference between abandoning a food source or remaining and continuing to feed. This is especially true in instances where the food item is nutritious, such as fruit. Sifakas, consuming mainly leaves, don’t have a lot of competition from other troops of sifakas or from other primate species. However, there can still be instances where one sifaka will displace another sifaka over a valued food item, such as flowers. More members in the group means greater competition within the group.

This is one of the disadvantages of group living. Living in a group also means that primates must get along with each other. Just think of a time when you didn’t get along with a sibling or a roommate. Energy must be invested in maintaining harmony within the group. Sifakas usually get along pretty well with each other, from what I have observed. There isn’t a whole lot of social interaction. I’ve only seen some sort of aggression a few times, usually a quick squabble over food. I’ve seen the sub-adults play wrestling with each other twice now, but otherwise these primates mainly feed, rest, and groom themselves.

Troop clinging to trees

Madagascar is a unique country in that there are no cat species on this island. There are no lions or leopards to worry about. The closest animal this island has to anything resembling a lion is the fossa, which is actually not a member of the felid family at all but a member of the civet family. Fossas are small but they will hunt and kill lemurs. There are no fossas in this part of Madagascar though, so the primates in Berenty need not worry. Their main concern comes from aerial predators. Large group size protects them from predatory birds, as do other strategies, such as feeding lower in the canopy, which I’ve observed both the smaller ring-tailed lemurs and brown lemurs doing. Sifakas are relatively large, which may be part of the reason they feel safe feeding on the tops of trees.

Mother with infant on back feeding on leaf buds

Many variables affect the size of a primate’s group: food availability, space, predation, etc. If the local habitat is reduced drastically by human activity, a primate may not be able to disperse into new territory to find mating opportunities outside of its natal group, causing tension and aggression within the group.

Critical thinking: Can you think of other instances in which human activity may affect the group size of a primate population?