No Surrender: Monkeys Fight Back Against Predators, But At What Cost?

ResearchBlogging.org One May morning in 2009, a group of white-faced capuchins were foraging on a hillside on Barro Colorado Island, Panama. Two researchers from the Smithsonian Tropical Research Institute, Anyuri González and Lucia Tórrez, were watching the group from nearby, but when one of the monkeys started shrieking, they realized they weren’t the only voyeurs.

The screams were an alarm call indicating a predator on the ground. The group’s alpha male took off in the direction of the noise and was joined several other adult members of the group, and they all began making facial and vocal threats and shaking and throwing branches toward a dense tangle of liana vines.

There was something in there, and the monkeys didn’t like it.

Mob Rules

While many animals go to great lengths to hide or flee from predators, some animals take the opposite tack and confront their attackers. Some species of primates, birds, fish and squirrels will harass and assault potential predators with mobbing behavior that involves loud vocalizations and physical attacks at close range.

The mobbing of a predator by capuchins is a real sight. Led by adult and subadult males, the monkeys will make loud threat and alarm calls while breaking large branches from trees and dropping them on the predator like bombs.

Researchers have been mistaken as predators themselves and received blows – at least one admitted to being knocked unconscious – from branches broken and dropped over their heads. Scientists working in capuchin territory quickly learn to to stop taking data and get out of the way when they see a monkey scanning the canopy directly above them, a sign that its looking for a branch that it will be able to break.

Some monkeys will get closer to predators if the aerial assault doesn’t work. In 1988, biological anthropologist Susan Boinski watched as a group of capuchins in Costa Rica killed a terciopelo, or fer-de-lance, after pinning it to the ground with a heavy branch and then approaching on the ground to beat it with sticks. One monkey rained down a flurry of 55 strikes to the snake’s body and head with a stick that it clumsily wielded like a club. Boinsky later approached the snake and found a mangled mess of bleeding wounds, exposed tissue and broken bones.

A Death in the Family

As González and Tórrez watched, a sense of alarm spread through the capuchin group. Juvenile monkeys and an adult female with a clinging infant gathered some distance away from the liana tangle, while the rest of the adults joined the alpha male on the frontline.

The capuchins’ alarm calls intensified and González, who was downwind from the liana tangle, noticed a distinct smell. A cat. She could see the right side of whatever was in the liana, and based on its size and fur color and patterns, decided it was not one the ocelots normally seen on the island, but a jaguar visiting from the mainland.

The cat growled loudly, making the capuchins visibly nervous. They glanced repeatedly at one another and one of the adult females retreated to where the juveniles were waiting. Together, they moved further away from the liana. The jaguar growled again and moved around in its hiding spot, and most of the remaining capuchins also retreated.

As far as González and Tórrez could see, only six adult and subadult males remained near the liana tangle, and their vocalizations had decreased in both frequency and intensity. They looked back and forth at one another and then moved silently away from the jaguar, following their groupmates.

Only one monkey stayed behind, and continued to make alarm calls. González and Tórrez weren’t able to see the monkey, and as they attempted to get close enough to verify which one it was, the cat made a very loud, very aggressive growl, and the researchers decided to retreat a little themselves.

From a safer distance, they could still hear the lone capuchin making alarm calls. Then, there was the sound of sudden movement and the rustling of branches. The alarm calls stopped and they heard two weak moans.

After that, there was only silence.

González and Tórrez encountered the capuchin group later that morning. The group was quiet, and had returned to foraging for insects. They took a headcount and found that one of the subadult males, named LK, was missing. Every other group member was accounted for but LK was not seen again over the course of their study.

At What Cost?

Approaching and mobbing predators appears to invite some obvious risks, as LK’s death shows. The true costs of mobbing are hard to suss out, though, because reports of primates being injured or killed while mobbing are very rare. The LK incident is, as far as González, Tórrez and their colleagues know, the first documented fatality arising from a mobbing event.

With limited observations, researchers have hypothesized several risks. The risk of injury and/or death seems to depend somewhat on the predator. Many snakes are cryptic hunters, and, once discovered, will freeze and can be mobbed with relatively little risk. Other predators, like large cats, continue to pose a significant threat to monkeys even after they’ve been discovered, and some will even chase their prey into the trees, giving them no quarter.

There are also other less grisly losses to consider, like the effort that goes into fighting back and opportunity costs of taking time from other activities. Some monkeys have been known to remain at the site of a spotted, attacked or even injured or dead predator for up to two hours after mobbing. That’s time and energy that could be spent foraging or mating sacrificed to a risky behavior, and even a “win” for mobbers might compromise the animals’ health and reproductive success, making it a Pyrrhic victory.

Figuring out the costs of mobbing, in turn, would help explain its benefits. If the price that primates are willing to pay to harass their predators are as large and varied as they seem, the rewards should be enough to make the risk worthwhile.

The obvious benefit of mobbing for social primates is that chasing off or killing predators helps protect their social group, relatives, mates and offspring. It’s also possible that mobbing events act as a learning opportunity for younger monkeys. Juveniles are able to study the animals that provoke alarm calls and defensive behavior and compare them to animals that don’t, and learn to know danger when they see it.

Another benefit to mobbing may be that, because it is so costly, it acts as an honest signal of an individual monkey’s quality as a mate. Attacking a predator gives a monkey the opportunity to display their physical condition, agility, and speed. Mobbing might be a way for females to evaluate the ability and willingness of males to protect them and their future offspring against threats.

Unfortunately, with so little data from the field or the lab, we don’t know how often mobbing ends lethally, or the likeliness of a fatal attack when a primate does vs. doesn’t mob, so it’s hard to weigh the costs and benefits that play on a monkey’s decision to stand its ground or retreat, maybe to fight another day.

References:
S. Boinski (1988). Use of a Club by a Wild White-Faced Capuchin (Cebus capucinus) To Attack a Venomous Snake (Bothrops asper) American Journal of Primatology, 14 (2), 177-179 DOI: 10.1002/ajp.1350140208

Tórrez, L., Robles, N., González, A., & Crofoot, M. (2012). Risky Business? Lethal Attack by a Jaguar Sheds Light on the Costs of Predator Mobbing for Capuchins (Cebus capucinus) International Journal of Primatology, 33 (2), 440-446 DOI: 10.1007/s10764-012-9588-1

Dugatkin, L., & Godin, J. (1992). Prey approaching predators: a cost-benefit perspective. Ann. Zool. Fennici, 29, 233-252

Lloyd, E., Kreetiyutanont, K., Prabnasuk, J., Grassman, L., & Borries, C. (2006). Observation of Phayre’s leaf monkeys mobbing a clouded leopard at Phu Khieo Wildlife Sanctuary (Thailand) Mammalia, 70 (1/2), 158-159 DOI: 10.1515/MAMM.2006.028

Caro, T. Antipredator Defenses in Birds and Mammals. University of Chicago Press. 2005.

Fragaszy, D., Visalberghi, E., Fedigan, L. The Complete Capuchin. Cambridge University Press. 2004.

Images: “Deux capucins moines Cebus capucinus” by Jean-Baptiste LECA & Noëlle Gunst. Public Domain. “Jaguar at the Belieze Zoo” by Bjørn Christian Tørrissen, used under a Creative Commons License.

 

 

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Stop, Hey What’s That Sound?: Chimps Know Social Upheaval When they Hear it.

ResearchBlogging.orgThe “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. [Read more]

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Context is King: Squirrels’ bodies react differently to warnings about different predators

ResearchBlogging.org

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 themselves or run/fly/swim like hell. Maybe a squirrel’s body 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 the 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 whistle alarms, trill alarms, 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. The change in cortisol levels compared to the baseline was only significant in response to the playback of the trill alarm calls. 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 air 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, however, 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 a hiding spot.

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

Both of these physiological reactions increase arousal and attention in a variety of species, so both might also just 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.

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Eavesdropping ungulates use baboon alarms to avoid predators

ResearchBlogging.org362258071_111a8114d8To 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

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Blue Whales going to farther depths

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.

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