Howler Monkeys and Harpy Eagles: A Communication Arms Race

  • Ricardo Gil-da-Costa
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Predation is considered by many researchers to be a selective pressure and strong evolutionary driving force in natural ecosystems. Predation phenomena are dynamic interactions that by definition need more than one agent: at least one predator and one prey. The interaction gets exponentially more complicated when we consider multiple agents and different strategies. These predator-prey interactions can be viewed as evolutionary arms races. There have been numerous studies on prey adaptations (Blumstein et al., 2000; Hauser & Caffrey, 1994; Marler et al., 1992; Endler, 1991; Cheney & Seyfarth, 1990; Hauser & Wrangham, 1990; Ryan et al., 1982), but few report both detailed adaptive responses to predation and ways predators can improve their killing efficiency (Berger et al., 2001). This lack of knowledge is even more striking for predation upon primates (Shultz et al., 2004; Gil-da-Costa et al., 2003; Zuberbühler, 2000a; Zuberbühler et al., 1999).


Alarm Call Howler Monkey Bald Eagle Barro Colorado Island Playback Stimulus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Baldwin, J.D. and Baldwin, J.I. (1976). Vocalizations of howler monkeys (A. palliata) in southwestern Panama. Folia primatol., 26: 81–108.PubMedGoogle Scholar
  2. Berger, J., Swenson, J.E., and Persson, I. (2001). Recolonizing carnivores and naïve prey: Conservation lessons from Pleistocene extinctions. Science, 291: 1036–1039.PubMedCrossRefGoogle Scholar
  3. Blumstein, D.T., Daniel, J.C., Griffin, A.S., and Evans, C.S. (2000). Insular tammar wallabies (Macropus eugenii) respond to visual but not to acoustic cues from predators. Behav. Ecol., 11(5): 528–535.CrossRefGoogle Scholar
  4. Boesch, C., and Boesch, H. (1989). Hunting behavior of wild chimpanzees in the TaÏ National Park. Amer. Jour. of Phys. Anthropol., 78: 547–573.CrossRefGoogle Scholar
  5. Boye, M., Gunturkun, O., and Vauclair, J. (2005). Right ear advantage for conspecific calls in adults and subadults, but not infants, California sea lions (Zalophus californianus): Hemispheric specialization for communication? European Jour. of Neuroscience, 21: 1727–1732.Google Scholar
  6. Brown, L., and Amadon, D. (1968). Eagles, hawks and falcons of the world. Vol. 2. New York: McGraw-Hill Book Co.Google Scholar
  7. Bshary, R. (2001). Diana monkeys, Cercopithecus diana, adjust their anti-predator response behaviour to human hunting strategies. Behav. Ecol. Sociobiol., 50: 251–256.CrossRefGoogle Scholar
  8. Caro, T.M. (1995). Pursuit-deterrence revisited. Trends Ecol. Evol., 10: 500–503.CrossRefGoogle Scholar
  9. Carpenter, C.R. (1965) The howlers of Barro Colorado Island. In I. DeVore (Ed.). Primate behavior. Field studies of monkeys and apes (pp. 250–291). New York: Holt, Rinehart and Winston Inc.Google Scholar
  10. Cheney, D.L., and Seyfarth, R.M. (1990). How monkeys see the world. Chicago: Chicago Univ. Press.Google Scholar
  11. Chivers, D.J. (1969). On the daily behaviour and spacing of howling monkey groups. Folia Primatol. (Basel), 10: 48–102.CrossRefGoogle Scholar
  12. Cords, M. (1990) Vigilance and mixed-species association of some East African forest monkeys. Behav. Ecol. Sociobiol., 26: 297–300.CrossRefGoogle Scholar
  13. Endler, J.A. (1991). Interactions between predators and prey. In J.R. Krebs and N.B. Davies (Eds.), Behavioral ecology (pp. 169–202). Oxford: Blackwell Scientific Publications.Google Scholar
  14. Fowler, J.M., and Cope, J.B. (1964). Notes on the harpy eagle in British Guiana. The Auk, 81: 257–273.Google Scholar
  15. Froehlich, J.W., Thorington, R.W., and Otis, J.S. (1981). The demography of howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. Inter. Jour. Primatol., 2: 207–236.Google Scholar
  16. Fullard, J.H., Dawson, J.W., and Jacobs, D.S. (2003). Auditory encoding during the last moment of a moth’s life. Jour. Exp. Biol., 206: 281–294.CrossRefGoogle Scholar
  17. Ghazanfar, A.A. (Ed.). (2003). Primate audition: Ethology and neurobiology. Boca Raton: Florida: CRC Press.Google Scholar
  18. Gaulin, S.J.C., Knight, D.H., and Gaulin, C.K. (1980). Local variance in Alouatta group size and food availability on Barro Colorado Island. Biotropica, 12: 137–143.CrossRefGoogle Scholar
  19. Gifford, G.W., MacLean, K.A., Hauser, M.D., and Cohen, Y.E. (2005). The neurophysiology of functionally meaningful categories: Macaque ventrolateral prefrontal cortex plays a critical role in spontaneous categorization of species-specific vocalizations. Jour. Cog. Neurosci., 17: 1471–1482.CrossRefGoogle Scholar
  20. Gil-da-Costa, R., Palleroni, A., Hauser, M.D., Touchton, J., and Kelley, J.P. (2003). Rapid acquisition of an alarm response by a Neotropical primate to a newly introduced avian predator. Proc. Roy. Soc. Lond. B, 270: 605–610.CrossRefGoogle Scholar
  21. Gil-da-Costa, R., Braun, A., Lopes, M., Hauser, M.D., Carson, R.E., Herscovitch, P., and Martin, A. (2004). Toward an evolutionary perspective on conceptual representation: Species-specific calls activate visual and affective processing systems in the macaque. Proc. Natl. Acad. Sci. USA, 101: 17516–17521.PubMedCrossRefGoogle Scholar
  22. Gittleman, J.L., and Gompper, M.E. (2001) The risk of extinction—What you don’t know will hurt you. Science, 291: 997–999.PubMedCrossRefGoogle Scholar
  23. Hasson, O. (1991). Pursuit-deterrent signals: Communication between prey and predators. Trends Ecol Evol., 6: 325–329.CrossRefGoogle Scholar
  24. Hauser, M.D., and Wrangham, R.W. (1990). Recognition of predator and competitor calls in non-human primates and birds: A preliminary report. Ethology, 86: 116–130.CrossRefGoogle Scholar
  25. Hauser, M.D. and Andersson, K. (1994). Left hemisphere dominance for processing vocalizations in adult, but not infant, rhesus monkeys: Field experiments. Proc. Natl. Acad. Sci., 91: 3946–3948.PubMedCrossRefGoogle Scholar
  26. Hauser, M.D., and Caffrey, C. (1994). Anti-predator response to raptor calls in wild crows, Corvus brachyrhynchos hesperis. Anim. Behav., 48: 1469–1471.CrossRefGoogle Scholar
  27. Heinsohn, R.P., and Craig, P. (1995). Complex cooperative strategies in group-territorial African lions. Science, 269: 1260–1262.PubMedCrossRefGoogle Scholar
  28. Hoy, R., Nolen, T., and Brodfuehrer, P. (1989). The neuroethology of acoustic startle and escape in flying insects. Jour. Exp. Biol., 146: 287–306.Google Scholar
  29. Jim, K.C., and Giles, C.L. (2000). Talking helps: Evolving communicating agents for the predator-prey pursuit problem. Artif. Life, 6: 237–254.PubMedCrossRefGoogle Scholar
  30. Mann, D.A., Lu, Z., Hastings, M.C., and Popper, A.N. (1998). Detection of ultrasonic tones and simulated dolphin echolocation clicks by a teleost fish, the American shad (Alosa sapidissima). Jour. Acoust. Soc. Am., 104: 562–568.CrossRefGoogle Scholar
  31. Mann, D.A., Lu, Z., and Popper, A.N. (1997). A clupeid fish can detect ultrasound. Nature, 389: 341.CrossRefGoogle Scholar
  32. Marler, P., Evans, C.S., and Hauser, M.D. (1992). Animal signals: Reference, motivation or both? In H. Papoucek, U. Jurgens, and M. Papoucek (Eds.), Nonverbal vocal communication: Comparative and developmental approaches (pp. 66–86). Cambridge: Cambridge Univ. Press.Google Scholar
  33. McGregor, P.K. (Ed.). (2005). Animal communication networks. Cambridge: Cambridge Univ. Press.Google Scholar
  34. Milton, K. (1980). The foraging strategy of howler monkeys. New York: Columbia Univ. Press.Google Scholar
  35. Milton, K. (1996) Effects of bot fly (Allouattamya baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. Jour. Zool. Lond., 239: 39–63.Google Scholar
  36. Palleroni, A., and Hauser, M.D. (2003). Experience-dependent plasticity for auditory processing in a raptor. Science, 299: 1195.PubMedCrossRefGoogle Scholar
  37. Palleroni, A. in prep. Harpy eagle development and behaviour.Google Scholar
  38. Poremba, A., Malloy, M., Saunders, R.C., Carson, R.E., Herscovitch, P., and Mishkin, M. (2004). Species-specific calls evoke asymmetric activity in the monkey’s temporal poles. Nature, 427: 448–451.PubMedCrossRefGoogle Scholar
  39. Rettig, N. (1978) Breeding behavior of the harpy eagle (Harpia harpyja). The Auk, 95: 629–643.Google Scholar
  40. Roeder, K.D. (1975). Neural factors and evitability in insect behavior. Jour. Exp. Zool., 194: 75–88.CrossRefGoogle Scholar
  41. Ryan, M.J., Tuttle, M.D., and Rand, A.S. (1982). Bat predation and sexual advertisement in a Neotropical frog. American Naturalist, 119: 136–139.CrossRefGoogle Scholar
  42. Rydell, J. (1998). Bat defence in lekking ghost swifts (Hepialus humuli), a moth without ultrasonic hearing. Proc. Biol Sci., 265: 1373–1376.PubMedCrossRefGoogle Scholar
  43. Schaller, G.B. (1972). The Serengeti lion: A study of predator-prey relationships. Chicago: Univ. Chicago Press.Google Scholar
  44. Sekulic, R., and Chivers, D.J. (1986). The significance of call duration in howler monkeys. Inter. Jour. Primatol., 7(2): 183–190.Google Scholar
  45. Seyfarth, R.M., Cheney, D.L., and Marler, P. (1980). Vervet monkey alarm calls: Semantic communication in a free-ranging primate. Animal Behaviour, 28: 1070–1094.CrossRefGoogle Scholar
  46. Seyfarth, R.M., and Cheney, D.L. (2003). Signalers and receivers in animal communication. Annu. Rev. Psychol., 54: 145–173.PubMedCrossRefGoogle Scholar
  47. Shultz, S., Noë, R., McGraw, W.S., and Dunbar, R.I. (2004). A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition. Proc. R. Soc. Lond. B., 271: 725–732.CrossRefGoogle Scholar
  48. Stanford, C.B. (1998). Chimpanzee and red colobus: The ecology of predator and prey. Cambridge, MA: Harvard Univ. Press.Google Scholar
  49. Struhsaker, T.T. (1967). Auditory communication among vervet monkeys. In S.A. Altman (Ed.), Social communication among primates (pp. 281–324). Chicago: Univ. Chicago Press.Google Scholar
  50. Touchton, J.M., Hsu, Y. and Palleroni, A. (2002). Foraging ecology of captive-bred subadult harpy eagles (Harpia harpyja) on Barro Colorado Island, Panama. Ornitologia neotropical, 13: 365–379.Google Scholar
  51. Treves, A. (1997). Self-protection in primates. Doctoral. Harvard University.Google Scholar
  52. Willis, E.O., and Eisenmann, E. (1979). A revised list of birds of Barro Colorado Island, Panama. Smithsonian Contributions to Zoology, 291: 1–31.Google Scholar
  53. Wong, M., and Ventocilla, J. (1995). A day in Barro Colorado Island. Panama: Smithsonian Tropical Research Institute.Google Scholar
  54. Woodland, D.J., Jaafar, Z., and Knight, M.L. (1980). The ‘pursuit-deterrent’ function of alarm signals. American Naturalist, 115: 748–753.CrossRefGoogle Scholar
  55. Zuberbühler, K., Jenny, D., and Bshary, R. (1999). The predator deterrence function of primate alarm calls. Ethology, 105: 477–490.Google Scholar
  56. Zuberbühler, K. (2000a). Causal knowledge of predators’ behaviour in wild Diana monkeys. Animal Behaviour, 59: 209–220.PubMedCrossRefGoogle Scholar
  57. Zuberbühler, K. (2000b). Interspecies semantic communication in two forest primates. Proc. R. Soc. Lond. B, 267: 713–718.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Ricardo Gil-da-Costa
    • 1
  1. 1.Laboratory of Brain and CognitionNational Institute of HealthBethesdaUSA

Personalised recommendations