Giant Birds and Terrified Monkeys

[It's a really busy week over here at blog headquarters, because it is data collection week. Data collection week is awesome, but it means less time for blogging. So here's a piece from the archives. I picked this one especially for Drugmonkey, because he liked it so much.]

This post was chosen as an Editor's Selection for ResearchBlogging.orgResearchBlogging.orgThe Harpy Eagle (Harpia harpyja) is a nasty scary-looking muppethugging monster of a carnivorous bird. Female harpies weigh 14-20 pounds, and males weigh 8.5-12 pounds. They stand between 2.9 and 3.5 feet tall. The wingspan of the harpy eagle can reach 6 feet, 7 inches. The talons - sharp claws to grasp onto its prey - are up to 5.1 inches long. INCHES!!

Figure 1: Yikes.

Figure 2: As tall as a small child.
Figure 3: I would not want to be on the receiving end of those talons.

Figure 4: Muppets make everything better.

These are scary, scary birds. They eat meat. They mainly hunt sloths, monkeys, porcupines, anteaters, iguanas, and opossums, but they also have been known to hunt other birds. They also sometimes hunt wolves and deer. Have I convinced you yet that these are nasty scary monster birds?

No? Watch this.

Okay, so relatively little has been known about how predators hunt primate prey, and how primates acquire adaptive responses to counteract predation. Predator-prey interactions are often viewed as evolutionary arms races - so if a new predator was introduced to a population of primates which previously had no real predators to speak of - would it lead to an adaptive anti-predator response? How would it emerge?

Barro Colorado Island (BCI), in the middle of the Panama Canal, has been a biological reserve since 1923, continuously monitored by resident biologists for almost 90 years. During that time, no harpy eagles had resided on BCI. Several primate species lived on the island, however, including howler monkeys, capuchins, spider monkeys, and Geoffrey's marmosets. We'll focus on the howler monkeys, who lived in approximately 65 troops, each with an average of 19 members.

Figure 5: A pair of howler monkeys.

Other than occasional visits from boa constrictors and large cats, these non-human primates had no relevant predators; the most important regulator of the howler population was most likely disease


Two radio-tagged harpy eagles were introduced to the island (for reasons unrelated to this research).

The adult male harpy was released in June 1999, when he was 19 months old. The adult female was released in October 1999, at 20 months of age. The current study began after the eagles had been on the island 12 and 8 months, respectively. During their stay at BCI, the eagles flew and hunted over the entire island, but favored the western side, spending 75% of their time in that area.

The expectation was that in that time (~1 year), the presence of the harpy eagles would have stimulated the rapid emergence of an alarm response among the howler monkeys. The researchers took advantage of the fact that harpies make a loud species-specific vocalization prior to attacking their prey. This call is not only associated with their presence, but with their potential threat as a predator. It is also known that other primate groups in other locations recognize predators on the basis of acoustic cues alone. So by playing back pre-recorded harpy calls, they could observe and record any anti-predator alarm calls made by the monkeys.

There were four experimental conditions:
(1) BCI Harpy Present: Howler monkeys from BCI presented with harpy calls, during a period in which harpies were present on the island.
(2) Gigante Control: Howler monkeys from a different location, the Gigante peninsula, who have not been exposed to harpies in the last 50-100 years, were presented with harpy calls. They two groups of howler monkeys and locations were very similar; both had no natural predators. The only significant difference was the reintroduction of harpies to BCI.
(3) BCI Harpy Absent: Howler monkeys from BCI presented with harpy calls during a later period, after the two harpies were removed from the island. The harpies were removed from the island for reasons independent of this research.
(4) BCI Control: BCI howler monkeys presented with the attack calls of other birds.

Based on data from the radio transmitters, it was clear that the harpies were hunting capuchins and howler monkeys with great success. During a period of 294 days when nearly all kills were observed, the female harpy captured prey every 4.39 days, and the male every 3.71 days. Primates were taken 34.78% of the time by the female, and 12% of the time by the male. The clear majority of primate kills were howler monkeys (81% for the female, and 100% for the male). All howler troops were exposed to predation by the harpy eagles, many times.

If some experience with harpy predation is necessary to develop the alarm calls, then BCI howlers should show a response to the harpy calls (condition 1 and 3), but not to other stimuli (condition 4). Also, Gigante howlers should not show a response to the harpy calls, if experience with harpies is required (condition 2).

Figure 6: Vigilance rates before, during, and after a harpy playback. Filled bars are BCI Harpy Present; hatched bars are Gigante Control.

Figure 7: Vigilance rates before, during, and after playback. Open bars are Gigante control; filled bars are BCI control; hatched bars are BCI Harpy Absent.

First, compare the filled and hatched bars in figure 7. There was no evidence of increased vigilance when presented with vocalizations from a different bird species. This suggests that the alarm response in the howler monkeys was specific to the harpy eagles.

Next, examine the filled bars in figure 6. It is clear that after only a few months, the monkeys had learned to associate the harpies' attack call with the risk of predation, and developed an alarm response.

Check out the hatched bars in figure 7. The response to the harpy calls was maintained, even in their absence, for at least seven months following the removal of the harpies from the island.

Figure 8: Vigilance of howler monkeys in the various conditions. Open bars are during playback; filled bars are after playback.

The howler monkeys in the BCI harpy present and BCI harpy absent conditions showed no difference in vigilance rates during and after playback, while Gigante howlers showed a significant decrease in vigilance. The initial vigilance in the Gigante monkeys may represent a response to novelty, rather than a specific anti-predator response.

Further analyses indicated that, following playback, the BCI howlers scanned by looking upwards for the predator. The Gigante howlers merely oriented towards the sound coming from the speaker. This suggests that the BCI howlers had specific recognition of the threat imposed by the harpies' call. It also suggests that the BCI howlers did not simply expand an already-existing alarm call ("danger!") to include this new threat. Instead, a specific alarm call unique for harpy eagles was used: "Danger from above!"

Another analysis showed sex differences in response to harpy calls by BCI howlers, but not among Gigante howlers. Specifically, the adult females on BCI would pick up their infants and move towards the more dense areas of the jungle canopy. The adults males dispersed and moved farther away from the group and gave alarm calls. Presumably this increased the spatial extent of the area monitored by the male monkeys, for quicker recognition of the predator.

The results from this study parallel results from a similar study involving moose populations and wolf predation (full text PDF here). Specifically, prey that were unfamiliar with a predator for 50-100 years had lost their ability to recognize the calls of that predator, thus becoming extremely vulnerable to predation upon the re-introduction of that predator. But after exposure to the predator, the populations quickly learned how to recognize impending danger. They developed behavioral adjustments to counteract the risk of predation in an extremely short period (less than one year), indicating an ability to rapidly process predator-related information in less than one generation.

This study also provided important information regarding the predation behavior of harpy eagles. Whenever the prey's response was coordinated and whenever vigilance was maintained, the harpy either delayed its attack or moved on to a different target. However, when the response was chaotic and vigilance was minimal, the harpy attacked or moved closer to the target.

Another reason that this study is important, I think, is that large carnivores are increasingly becoming extinct (the harpy eagle is "near threatened"). This has left various prey (primates included) without selective predatory pressure and without the need to acquire self-protective behaviors. It is important, therefore, to understand various species' ability to reactivate anti-predator responses following reintroduction. Many conservationists are interested in or are exploring ways of reintroducing predators into their historical habitats; playbacks of predator calls could be used to assess the presence or absence of evolved anti-predation responses in prey animals. This information would be important in designing conservation programs.

How about some more scary pictures of harpy eagles?

Figure 9: I won't call this a glove. This is the apparatus that the handler has to wear to protect his arm from those massive talons.

Figure 10: Check out that wingspan.

Figure 11: Harpy eagle feeds on a rabbit. Circle of life, man.

Gil-da-Costa R, Palleroni A, Hauser MD, Touchton J, & Kelley JP (2003). Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator. Proceedings. Biological sciences / The Royal Society, 270 (1515), 605-10. PMID: 12769460


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Eating rabbit! cool!

I love your blog, everything here is absolutely fascinating. Keep going, I need more input!
BTW, I am wondering about the parallel between the howlers and humans, in their sex-divided responses where the females retreat into the denser forest and the males spread out around the perimeter. Are the males trying to protect the young (their possibly offspring) by leading the predators away, or are they trying to diffuse the threat to the entire group by making themselves scarce? What is the attitude of the males to their offspring? Do you have any links or more info on the subject? I could keep reading this stuff for hours!


Are the males trying to protect the young (their possibly offspring) by leading the predators away, or are they trying to diffuse the threat to the entire group by making themselves scarce?

The authors don't really speculate on this. My speculation is that the females take the children and huddle together in the thicker part of the trees where it's a bit safer, while the males form a protective perimeter to guard the group.

Perhaps the dispersal of the males is a multi-faceted defense mechanism. Not only does it provide multiple angles and therefore enhanced observation of the threat but it may also be effective in dissuading attack as it forces the eagle to select a specific target instead of having multiple options aggregated into a relatively small area. Additionally, it may be that the alarm calls of dispersed howlers are more effective in disturbing a predator than those of a closely assembled group.

It would be interesting to observe eagle reactions and attack patterns in response to this defense.

Are the males trying to protect the young (their possibly offspring) by leading the predators away, or are they trying to diffuse the threat to the entire group by making themselves scarce?

Why leap to the conclusion that they're not simply running away to hide? Not saying there mightn't be a positive effect through a kin- or group-selection mechanism, but that wouldn't mean the main effect of the response is not an individual survival advantage, or that the motive is not pure terror without the least altruistic consideration flitting through their skulls.

By John Scanlon, FCD (not verified) on 10 May 2010 #permalink

Well at least if you were a harpy eagle you could be on the delivery end of those talons

By Wildbirdr (not verified) on 20 Jun 2010 #permalink

Out of curiosity, why were the vigilance levels prior to the playing of the recording so much higher in the Gigante howlers than the BCI Harpy Present group? 30% seems like a great deal of a gap. Was it a reaction to the presence of the researchers?

By Tor Bertin (not verified) on 25 Sep 2010 #permalink

I enjoy your blog, and today's discussion with Johnson was very interesting. I'm writing, however, to inform you that the howler monkeys on Barro Colorado Island, Panama are Alouatta palliata, not A. caraya as depicted. A. palliata are not sexually dichromatic, both adult male and female having black pelage.

By Clara B. Jones (not verified) on 04 Dec 2010 #permalink