The “Ooooooohhhh!” a human being cries out when they stub their toe might sound a pretty similar to the “Ooooooohhhh!” they cry out at the end of their mating ritual, but they two calls are different. An important part of human-to-human communication is our ability to extract information from context-specific calls and integrate it with other information we already have to make sense of what we’re hearing. It’s how we know, if we’re standing in one room and the TV is on in another, the difference between the scream of a serial killer’s victim in a slasher movie and the scream of a hero going into battle in an action blockbuster. We might not know what kind of movie is on in there, but we can at least identify which end of a blade the screamer might be on.

Katie Slocombe, a lecturer at the University of York’s psychology department, has spent her career tracing the evolution of different aspects of human language. More often than not, she finds herself starting with pants, grunts, hoots and hollers of chimpanzees. Many people find this surprising, Slocombe has said, but they shouldn’t. Finding an evolutionary explanation for any part of human language is difficult. Unlike, say, wrist bones, spoken language hasn’t left any fossil remains behind for us to study. Genetic evidence from our hominid ancestors suggests that we evolved our capacity for complex spoken language in a very short window of time, so it’s likely that the cognitive abilities underlying language emerged farther back in the primate lineage. Hence it makes perfect sense to look to other living primates, apes and monkeys, for clues to language’s origins.

Chimpanzees, our closest living relatives, produce specific screams when locked in confrontation with each other. They vary their screams depending on their social role in a fight, with victims and aggressors producing acoustically distinct screams, and the victims additionally varying the structure of their screams based on amount of aggression they’re facing. Many things a listener would want to know about the conflict and the chimps involved is encoded in the sounds of the fight. Research has shown that chimps can discriminate the differences between these varying calls, and Slocombe wondered if they also share our ability to pull meaningful social information from them and make inferences about conflicts they can’t see.

To find their answer, Slocombe and her colleagues, Tanja Kaller, Josep Call and Klaus Zuberbühler, paid a visit to the chimpanzees living at the Wolfgang Köhler Primate Research Centre (WKPRC), Leipzig, Germany. They recorded screams from naturally occurring conflicts within the troop and monitored the responses of several bystander chimps to two types of scream sequences. One, the congruent sequence, consisted of calls that were in accordance with existing social dominance relations (that is, dominant animals were the aggressors and lower ranking ones were the victims), and the other, the incongruent sequence, consisted of calls that violated the hierarchy.

The researchers hypothesized that if chimps could discriminate and figure out the meaning of the different calls and the socialconstraints under which the two callers live, they would respond more to the latter sequences (in line with results from studies of other animals and human infants). If they couldn’t understand they context of the calls, their responses should be random, or in the other direction since, since the congruent sequences are more acoustically interesting.

The call of the wild

The incongruent call sequence consisted of a low-ranking chimp giving an aggressor scream, followed by a higher-ranking chimp giving a victim scream. This is an unusual event, because chimpanzees are rarely pushed around by lower-ranking group members. Congruent sequence would logically seem to consist of an inverted sequence, a high-ranking aggressor scream then low-ranking victim scream, but juxtaposing this with the incongruent sequence presented the problem of novelty. Because the incongruent sequence was so unusual, interpreting a strong response to it would be difficult. Did the bystander chimps respond because they could only understand the conflict by extracting social information from the calls, or simply because it was an unusual thing to hear?

To solve the problem, the researchers needed a workaround so that the sequences of aggressor and victim screams remained identical in the two conditions. For the congruent sequence, they reused the incongruent scream sequence, but added a third voice to the mix. The “pant-hoot” of a top-ranking male was slipped into the middle of the recording so that it overlapped with parts of the aggressor and the victim screams. Two of the screams were the same as the incongruent sequence, taking away from its novelty, and the third voice made the scenario socially plausible: it sounds like the high-ranking victim’s scream was elicited by the dominant male, rather than the low-ranking individual.

Smile, You’re on Candid Camera

Three males and seven females (10-31 years old) from the troop of 18 housed at the research center participated in the experiment. Each round involved 6-7 of the chimps as the one listening subject, two or three call providers or two “extras.” Assuming that the social chimps kept track of each other’s whereabouts, the researchers set up an elaborate deception to keep the experiment spatially realistic. For each trial, the listener was first separated from the scream providers and extras in the chimps’ compartmentalized sleeping room, where it could still see and hear them, and then released into another indoor room where it could only hear the others. After the subject was isolated in the other room for a few minutes, the screamers and extras were released into an outside area where wouldn’t hear their own calls being broadcast.

Since the subject would certainly hear the sound of the hydraulic doors and maybe associate it with release to the outside area, the chimps’ keeper then opened and closed some of the internal doors in the sleeping room and gave shouted commands, play-acting the procedure for moving chimps around in the room and creating the impression for the subject that some unknown chimps were still in there. The researchers then broadcast the call sequence recordings from the sleeping room (here’s a diagram of the chimps’ changing positions through the experiments). The subject’s response to the playback was filmed, and after five minutes the keepers simulated the release of the chimps from the sleeping room to the outdoor enclosure by shouting and operating the doors. The subject then rejoined the group in the outdoor enclosure.

While all this went on, the researchers measured (1) the duration the listener looked towards the sleeping room in the minute before the playback, (2) the duration he or she looked towards the sleeping room in the minute after the victim screams began (that is, where it became apparent whether the scream sequence was congruent or incongruent) and (3) whether the subject approached the sleeping room doors in the minute after playback.

Do you hear what I hear?

Comparing responses to the two scream sequences, the researchers found that eight of the ten chimps looked in the direction of the screams for an average of 3 seconds longer during the incongruent sequence than during the congruent one, one looked longer during the congruent sequence and one showed no discrimination between the two. Additionally, four of the chimps responded to the incongruent sequences by approaching the doors to the sleeping room; three of them did the same in response to the congruent sequence. Below is a chimp-by-chimp breakdown of the looking duration for each sequence.

The differences in looking responses couldn’t be explained away by the acoustic features of the call sequences. The chimps showed a weaker response to the congruent sequences even though these were more acoustically attention-grabbing and contained more call types from more individuals, including a top-ranking male, who generally evokes the most interest when a fight breaks out. Instead, the researchers think that the chimps’ stronger response to the incongruent sequences suggests that the chimps were figuring out the social roles of the two screamers and making sense of the conflict by putting the calls and the roles of the callers in a wider social context. Since the social upset happening in the incongruent interactions couldn’t be sussed out simply by the acoustic features of the call sequence; the listener would have to make some inferences about the direction of aggression by assigning two distinct social roles – victim and aggressor – to the screaming chimps and integrating that with their existing social knowledge about the expected social standing of the screamers. The fact that the chimps seem to have done so suggests 1) that our ability to read into screams, cries and other calls first appeared far back in our lineage and 2) that the gap that separates us from the rest of the animals has narrowed again.

Reference: Slocombe KE, Kaller T, Call J, & Zuberbühler K (2010). Chimpanzees extract social information from agonistic screams. PloS one, 5 (7) PMID: 20644722
Slocombe, K., Townsend, S., & Zuberbühler, K. (2008). Wild chimpanzees (Pan troglodytes schweinfurthii) distinguish between different scream types: evidence from a playback study Animal Cognition, 12 (3), 441-449 DOI: 10.1007/s10071-008-0204-x

Image: Chimpanzee at Oji zoo, Kobe, Japan, by Flickr user pelican. Used under a Creative Commons license.

One if by land, and two if by sea/And I on the opposite shore will be/Ready to ride and spread the alarm/Through every Middlesex village and farm/For the country folk to be up and to arm.

On April 18, 1775, Paul Revere told three Boston patriots to hang two lanterns in the steeple of the city’s Old North Church. A militia waiting across the Charles River in Charlestown kept an eye out for these signal lanterns and were prepared act appropriately as soon as they saw one or both of the lights stab out at the darkness. The meaning of the two lanterns has been memorized by countless American schoolchildren in the century and a half since Longfellow published “Paul Revere’s Ride.” One lantern told the militia that the British Army would march over Boston Neck and the Great Bridge, and two meant that that the Redcoats would take boats across the river to land near Phips farm.

Many, if not most, birds and mammals that live in groups have their own signals and alarms that alert members of the group to predators and other dangers. An alarm call can mean the difference between life and death for animals who didn’t detect the threat on their own and younger animals who are especially vulnerable to predation. Belding’s ground squirrels take a cue from Revere and use two different alarm calls to warn of two types of danger. Whistle alarm calls signal aerial predators and trill alarm calls signal terrestrial ones. A squirrel needs to react differently to each type of call and to each type of predator. Listeners respond to whistles by entering a burrow or another hiding spot, and adopt a “posting” stance on their hind legs in response to trills.

When young Belding’s squirrels first emerge from their burrows when they’re a month old, they don’t respond appropriately to the two different calls and if they respond at all, they typically just freeze. They pick up on the appropriate behavioral responses very quickly, though, often within five days of coming above ground. Watching the responses of mom, dad and the other squirrels could teach a youngster what they need to know pretty quickly, but Jill Mateo, from the Department of Comparative Human Development at the University of Chicago, wondered if there was also a physiological factor. For many species, the sight, sound or even odor of a predator spurs physiological changes that make individuals better prepared to track predators and the responses of other animals, hide and be still, defend itself or run/fly/swim like hell. Maybe the body itself reacts differently to a whistle than it does to a trill – to two lanterns than it does to one, if you will – and helps prime a squirrel for one response or another.

For the first five days after they come aboveground, juvenile ground squirrels show a higher level of cortisol (a steroid hormone released in response to stress) than during the days before emergence or the weeks after. To see if the hormone had some role in ground squirrels learning appropriate anti-predator behavior, Mateo tested how the levels of the hormone changed in response to different alarm and non-alarm calls. She caught pregnant female squirrels at a few sites near the Sierra Nevada Aquatic Research Laboratory (SNARL) at Mammoth Lakes, CA and brought them back to the lab so they could give birth and rear their young. Around the time the babies would normally leave the burrow, Mateo placed them, in pairs, in a large, dark wooden box once per day and played either a recording of ground squirrel whistles alarm, trill alarm calls, squeals young squirrels use during play or a silent control.

Every time a squirrel heard a recording, Mateo took a blood sample from it. These tests continued until she had one blood sample for each of the four recordings from a squirrel or until the squirrel turned 35 days old (in some cases, she was not able to get complete samples from a squirrel before it reached the age limit or did not have a large enough sample to analyze). After two rounds of tests in 2006 and 2008, Mateo had partial samples from 32 squirrels and complete samples from 17 of those.

Mateo analyzed the samples and, using a squirrel’s cortisol concentration following the silent stimulus as its baseline, looked at the hormone’s percent change in response to the alarm calls and play noises. Because multiple squirrels from several different litters were tested, Mateo averaged the cortisol responses to each recording for each litter.

For all litters, cortisol concentrations were higher following playback of trill alarm calls than after the other recordings (see graph above). The change in cortisol levels compared to the baseline was only significant in response to the playback of the trill alarm calls (graph below). The whistle alarms did not increase cortisol concentrations, but earlier research by Mateo showed that they do elicit bradycardia, a slower than normal heart rate.

So the squirrels do have different physiological responses to the two alarm calls. What relationship do these changes inside the body have with behavior, though, and what do they have to do with aerial versus ground attacks? Mateo hypothesizes that cortisol might not increase in response to whistles because attacks by avian predators often only last a few seconds and most birds don’t make repeated attacks if their first one is unsuccessful; the attack would be over before circulating cortisol increased. Bradycardia is associated in young squirrels with decreased motor activity and enhanced information processing. If the heart slows in response to whistles, the squirrels can stay still and pay attention in case it needs to make a break for another hiding spot.

The terrestrial predators that squirrels respond to with trills, on the other hand, usually spend a significant amount of time (up to 30 minutes) either moving around squirrel burrows or waiting near one to attempt an ambush. Increased cortisol makes glucose available as fuel, allowing for sustained vigilance in posting stances and, if needed, for multiple escape attempts.

Both of these physiological reactions increase arousal and attention in a variety of species, so both might simply aid young squirrels in noticing and paying attention to the responses that nearby adults have to the alarm calls, making for a faster association between the alarms and their appropriate responses.

References: Mateo JM (2010). Alarm calls elicit predator-specific physiological responses. Biology letters, 6 (5), 623-5 PMID: 20236965

Mateo JM (1996). Early auditory experience and the ontogeny of alarm-call discrimination in Belding’s ground squirrels (Spermophilus beldingi). Journal of comparative psychology (Washington, D.C. : 1983), 110 (2), 115-24 PMID: 8681525

Image: “Belding’s Ground Squirrel in the Sierra Nevada Mountains, California, USA” by Justin.Johnsen via Wikimedia Commons. Used under a Creative Commons Attribution 3.0 license.

To borrow from Jonah Lehrer (in turn, giving a nod to Hobbes Hobbes), “baboons are nasty, brutish and short.” They’re noisy little brutes, at that. When they encounter predators, females and juveniles produce harsh single-syllable barks (turn your volume up a little). During baboon-on-baboon fights or dominance contests, the women and children scream. In both situations, males produce two-syllable “wahoos.” All the ruckus doesn’t necessarily make them bad to have around, though. Many animals respond, often appropriately, to alarm calls produced by other species. This, “eavesdropping” behavior has been observed both within taxonomic groups (among birds, marmots and squirrels) and between them (some mammals and reptiles, vervet monkeys, red squirrels, Gunther’s dik-diks, banded mongooses and Galápagos marine iguanas among them, respond to bird calls; hornbills can discriminate among different primate alarm calls). If species that live in proximity to baboons have gotten the hang of telling alarm calls from contest ones and learned to associate alarm calls with predators, they might avoid becoming lunch thanks to their noisy neighbors.

On the Okavango Delta in northwestern Botswana, impala, tsessebe, zebra and wildebeest are all abundant, all hear baboon calls often and all respond to the baboons’ alarm calls. Although all four ungulates come into contact with baboons, only impala regularly intermingle with the apes at close range, likely because of their overlapping diet and habitat preferences. Baboons and impala also share a vulnerability to predation by leopards and lions, while the larger ungulates only have to worry about the lions. Impala, therefore, are more likely to experience a close juxtaposition of baboon alarm calls and appearance of predators and have more opportunity to associate the two.

To test what seems like the impala’s edge over the other species, Dawn Kitchen, James R. Nicholson (Ohio State University), Thore Bergman (University of Michigan), Dorothy Cheney and Robert Seyfarth (University of Pennsylvania) broadcasted four unique pairs of baboon call sequences – each pair consisted of one sequence of alarm calls recorded during a lion encounter and one sequence of calls recorded during a male-male altercation that involved the chasing of females and juveniles – in the presence of groups of the four ungulate species. All four species showed stronger responses (responses measured were latency to orient toward the speaker, duration of looking toward the speaker, latency to move at least 1 m and rate of moving) to the alarm call sequences than to the contest sequences (even though both sequence types were similar in pattern, amplitude and duration). The impala, though, had stronger response scores than all other species combined in both the alarm and contest conditions and demonstrated the strongest discrimination between the two call sequence types. Specifically, the impala observed showed shorter latencies to orient toward the speaker, looked toward the speaker for a longer duration, began moving sooner, and moved at faster rates after the playback of alarm calls than contest calls.

Do these ungulates possess an innate skill for telling the difference between baboon alarm calls and other calls, or do they learn, over time, to separate the signal from the noise? Were the ability innate in any of the species, the researchers say, it could be explained by an acoustic convergence between baboon alarm calls and the alarm calls of the ungulates. However, their alarm calls are made up primarily of snorts that have little in common with the baboons’ barks and wahoos. Instead of natural talent, the researchers think the ungulates learn to discriminate between baboon calls, given the impala’s strong response difference to the two baboon call sequences, the species exposure to baboons and available opportunity to associate alarm calls with danger. The researchers suggest that the ungulates’ responses were guided primarily by the alarm calls of the females and juveniles, which are easier to differentiate from other calls than the males’ alarm and contest wahoos (although, female baboons can differentiate male calls and there is some evidence that birds can parse the subtle differences, humans can’t discriminate the calls by ear). Familiarity and social learning have been implicated as mechanisms for interspecies call recognition in other research. Juvenile vervet monkeys residing in groups that regularly hear the alarm calls of superb starlings responded appropriately to playback of starling calls at a younger age than juvenile vervets living in groups with lower rates of exposure. To further test their hypothesis, Kitchen and her co-authors suggest a similar series of playback tests conducted on young ungulates with varying levels of exposure to baboons and their vocalizations.

Reference: Kitchen DM, Bergman TJ, Cheney DL, Nicholson JR, & Seyfarth RM (2010). Comparing responses of four ungulate species to playbacks of baboon alarm calls. Animal cognition PMID: 20607576

Image: “Chacma Baboon – Papio ursinus” by Flickr user Arno & Louise Wildlife

When you enjoy the simple pleasures that I do – heavy metal, zombie movies, all things Batman – it’s not often that life imitates art in a way that you can appreciate. Sometimes, though, Mother Earth will surprise me with just how cool she is.

Case in point: Generations of musicians have been taking Black Sabbath-esque riffs and dragging them to lower, slower depths. We’re at the point now where some of the best guitar riffs are just a single chord degrading over the course of a few minutes at 32Hz.

The songs of male blue whales, long thought to be the way they attract mates, have likewise been getting lower over the last 40 years, and in some populations have dropped in frequency by as much as 30 percent (mind you that whale songs were already mostly too low for human ears to hear).

Besides a desire to jump on the drone bandwagon before the Next Big Thing comes along, what could be prompting the whales to lower their songs so much, so quickly?

The scientists researching the trend can’t explain it, but hypothesize that it might be because the whale population is rebounding after years of commercial whaling bans, and with more whales around, a lower song gives a male an edge when attracting a mate.