Animal Cognition

, Volume 19, Issue 4, pp 789–797 | Cite as

Acoustic behavior associated with cooperative task success in bottlenose dolphins (Tursiops truncatus)

  • Holli C. EskelinenEmail author
  • Kelley A. Winship
  • Brittany L. Jones
  • Audra E. M. Ames
  • Stan A. KuczajII
Original Paper


Although many species have proven capable of cooperating to achieve common goals, the role of communication in cooperation has received relatively little attention. Analysis of communication between partners is vital in determining whether actions are truly cooperative rather than serendipitous or learned via trial and error (Chalmeau and Gallo in Behav Process 35:101–111, 1996a. doi: 10.1016/0376-6357(95)00049-6, Primates 37:39–47, 1996b. doi: 10.1007/BF02382918). Wild cetaceans often produce sounds during cooperative foraging, playing, and mating, but the role of these sounds in cooperative events is largely unknown. Here, we investigated acoustic communication between two male bottlenose dolphins while they cooperatively opened a container (Kuczaj et al. in Anim Cogn 18:543–550, 2015b. doi: 10.1007/s10071-014-0822-4). Analyses of whistles, burst pulses, and bi-phonations that occurred during four contexts (i.e., no container, no animals interacting with container, one animal interacting with container, and two animals interacting with container) revealed that overall sound production rate significantly increased during container interactions. Sound production rates were also significantly higher during cooperative successes than solo successes, suggesting that the coordination of efforts rather than the apparatus itself was responsible for the phonation increase. The most common sound type during cooperative successes was burst pulse signals, similar to past recordings of cooperative events in bottlenose dolphins (Bastian in Animal sonar systems. Laboratoire de Physiologie Acoustique, Jouy-en Josas, pp 803–873, 1967; Connor and Smolker 1996).


Cognition Cooperative behavior Sound production Communication Atlantic bottlenose dolphin Tursiops truncatus 



The authors would like to extend our gratitude to the Research and Animal Care/Training staffs at Dolphins Plus Bayside for their commitment to conducting trials and support of the study.


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267. doi: 10.1121/1.3177272 CrossRefPubMedGoogle Scholar
  2. Bastain J (1967) The transmission of arbitrary environmental information between bottlenose dolphins. In: Busnel RG (ed) Animal sonar systems. Laboratoire de Physiologie Acoustique, Jouy-en Josas, pp 803–873Google Scholar
  3. Beck BB (1973) Cooperative tool use by captive hamadryas baboons. Science 182:594–597. doi: 10.1126/science.182.4112.594 CrossRefPubMedGoogle Scholar
  4. Bel’Kovich VM, Ivanova EE, Yefremenkova OV, Kozarovitsky LB, Kharitonov SP (1991) Searching and hunting behavior in the bottlenose dolphin (Tursiops truncatus) in the black sea. Dolphin societies: discoveries and puzzles. University of California Press, Berkeley, pp 38–67Google Scholar
  5. Benoit-Bird KJ, Au WW (2003) Prey dynamics affect foraging by a pelagic predator (Stenella longirostris) over a range of spatial and temporal scales. Behav Ecol Sociobiol 53:364–373. doi: 10.1007/s00265-003-0585-4 Google Scholar
  6. Benoit-Bird KJ, Au WWL (2009) Cooperative prey herding by the pelagic dolphin, Stenella longirostris. J Acoust Soc Am 125:125–137. doi: 10.1121/1.2967480 CrossRefPubMedGoogle Scholar
  7. Blomqvist C, Amundin M (2004) High-frequency burst-pulse sounds in agonistic/aggressive interactions in bottlenose dolphins, Tursiops truncatus. In: Thoman JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 425–431Google Scholar
  8. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the Taï National Park. Am J Phys Anthropol 78:547–573. doi: 10.1002/ajpa.1330780410 CrossRefPubMedGoogle Scholar
  9. Bowles A, Grebner D, Musser W, Nash J, Crance J (2015) Disproportionate emission of bubble streams with killer whale biphonic calls: perspectives on production and function. J Acoust Soc Am 137:EL165–EL170. doi: 10.1121/1.4905882 CrossRefPubMedGoogle Scholar
  10. Bräuer J, Bös M, Call J, Tomasello M (2013) Domestic dogs (Canis familiaris) coordinate their actions in a problem-solving task. Anim Cogn 16:273–285. doi: 10.1007/s10071-012-0571-1 CrossRefPubMedGoogle Scholar
  11. Bullinger AF, Melis AP, Tomasello M (2011a) Chimpanzees, Pan troglodytes, prefer individual over collaborative strategies towards goals. Anim Behav 82:1135–1141. doi: 10.1016/j.anbehav.2011.08.008 CrossRefGoogle Scholar
  12. Bullinger AF, Wyman E, Melis AP, Tomasello M (2011b) Coordination of chimpanzees (Pan troglodytes) in a stag hunt game. Int J Primatol 32:1296–1310. doi: 10.1007/s10764-011-9546-3 CrossRefGoogle Scholar
  13. Caldwell MC, Caldwell DK (1965) Individualized whistle contours in bottlenose dolphins (Tursiops truncatus). Nature 207:434–435. doi: 10.1038/207434a0 CrossRefGoogle Scholar
  14. Caldwell MC, Caldwell DK (1966) Epimeletic (care-giving) behavior in Cetacea. In: Norris KS (ed) Whales, dolphins and porpoises. University of California Press, Los Angeles, pp 755–789Google Scholar
  15. Caldwell MC, Caldwell DK (1967) Intraspecific transfer of information via the pulsed sound in captive odontocete cetaceans. In: Busnel RG (ed) Animal sonar systems: biology and bionics. Jouy-en-Josas, Paris, pp 879–936Google Scholar
  16. Caldwell MC, Caldwell DK, Tyack PL (1990) Review of the signature-whistle hypothesis for the Atlantic bottlenose dolphin. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, pp 199–234CrossRefGoogle Scholar
  17. Chalmeau E (1994) Do chimpanzees cooperate in a learning task? Primates 35:385–392. doi: 10.1007/BF02382735 CrossRefGoogle Scholar
  18. Chalmeau R, Gallo A (1996a) Cooperation in primates: critical analysis of behavioural criteria. Behav Process 35:101–111. doi: 10.1016/0376-6357(95)00049-6 CrossRefGoogle Scholar
  19. Chalmeau R, Gallo A (1996b) What chimpanzees (Pan troglodytes) learn in a cooperative task. Primates 37:39–47. doi: 10.1007/BF02382918 CrossRefGoogle Scholar
  20. Chalmeau R, Lardeux K, Brandibas P, Gallo A (1997) Cooperative problem solving by orangutans (Pongo pygmaeus). Int J Primatol 18:23–32. doi: 10.1023/A:1026337006136 CrossRefGoogle Scholar
  21. Cockcroft VG, Sauer W (1990) Observed and inferred epimeletic (nurturant) behavior in bottlenose dolphins. Aquat Mamm 16:31–32Google Scholar
  22. Connor RC, Smolker RA (1996) ‘Pop’ goes the dolphin: a vocalization male bottlenose dolphins produce during consortships. Behaviour 133:643–662. doi: 10.1163/156853996X00404 CrossRefGoogle Scholar
  23. Connor RC, Smolker RA, Richards AF (1992) Two levels of alliance formation among male bottlenose dolphins (Tursiops sp.). Proc Natl Acad Sci 89:987–990. doi: 10.1073/pnas.89.3.987 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin: social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 91–126Google Scholar
  25. Crawford MP (1937) The cooperative solving of problems by young chimpanzees. Comp Psychol Monogr 14:1–88Google Scholar
  26. Cronin KA, Kurian AV, Snowdon CT (2005) Cooperative problem solving in a cooperatively breeding primate (Sanguinus Oedipus). Anim Behav 69:133–142. doi: 10.1016/j.anbehav.2004.02.024 CrossRefPubMedPubMedCentralGoogle Scholar
  27. de Moura JF, Rodrigues EDS, Siciliano S (2009) Epimeletic behavior in rough-toothed dolphins (Steno bredanensis) on the east coast of Rio de Janeiro State, Brazil. Mar Biodivers Rec 2:1–3. doi: 10.1017/S1755267208000122 CrossRefGoogle Scholar
  28. Drea CM, Carter AN (2009) Cooperative problem solving in a social carnivore. Anim Behav 79:967–977. doi: 10.1016/j.anbehav.2009.06.030 CrossRefGoogle Scholar
  29. Duffy-Echevarria EE, Connor RC, St. Aubin DJ (2008) Observations of strand-feeding behavior by bottlenose dolphins (Tursiops truncatus) in bull creek, South Carolina. Mar Mamm Sci 24:202–206. doi: 10.1111/j.1748-7692.2007.00151.x CrossRefGoogle Scholar
  30. D’Vincent CG, Nilson RM, Hanna RE (1985) Vocalization and coordinated feeding behavior of the humpback whale in southeastern Alaska. Sci Rep Whales Res Inst 36:41–47Google Scholar
  31. Hattori Y, Kuroshima K, Fujita K (2005) Cooperative problem solving by tufted capuchin monkeys (Cebus apella): spontaneous division of labor, communication, and reciprocal altruism. J Comp Psychol 119:335–342. doi: 10.1037/0735-7036.119.3.335 CrossRefPubMedGoogle Scholar
  32. Hirata S, Fuwa K (2007) Chimpanzees (Pan troglodytes) learn to act with other individuals in a cooperative task. Primates 48:13–21. doi: 10.1007/s10329-006-0022-1 CrossRefPubMedGoogle Scholar
  33. Hoese HD (1971) Dolphin feeding out of water in a salt marsh. J Mamm 52(1):222–223. doi: 10.2307/1378455 CrossRefGoogle Scholar
  34. Janik VM (2000) Food-related bray calls in wild bottlenose dolphins (Tursiops truncatus). Proc R Soc B 267:293–297. doi: 10.1098/rspb.2000.1091 CrossRefGoogle Scholar
  35. Janik VM, Sayigh LS (2013) Communication in bottlenose dolphins: 50 years of signature whistle research. J Comp Physiol A 199:479–489. doi: 10.1007/s00359-013-0817-7 CrossRefGoogle Scholar
  36. Janik VM, Slater PJB (1998) Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Anim Behav 56:829–838. doi: 10.1006/anbe.1998.0881 CrossRefPubMedGoogle Scholar
  37. Jones GJ, Sayigh LS (2002) Geographic variation in rates of vocal production of free-ranging bottlenose dolphins. Mar Mamm Sci 18:374–393. doi: 10.1111/j.1748-7692.2002.tb01044.x CrossRefGoogle Scholar
  38. Kellogg WN (1961) Porpoises and sonar. University of Chicago Press, Chicago, pp 159–168Google Scholar
  39. King SL, Janik VM (2015) Come dine with me: food-associated social signaling in wild bottlenose dolphins (Tursiops truncatus). Anim Cogn 18:969–974. doi: 10.1007/s10071-015-0851-7 CrossRefPubMedGoogle Scholar
  40. Kuczaj SA II, Highfill LE (2005) Dolphin play: evidence for cooperation and 468 culture? Behav Brain Sci 28:705–706. doi: 10.1017/S0140525X05370129 CrossRefGoogle Scholar
  41. Kuczaj SA II, Walker RT (2012) Dolphin problem solving. In: Zentall T, Wasserman E (eds) Handbook of comparative cognition. Oxford University Press, New York, pp 736–756Google Scholar
  42. Kuczaj SA II, Yeater D (2007) Observations of rough-toothed dolphin (Steno bredanensis) off the coast of Utila, Honduras. J Mar Biol Assoc UK 87:141–148. doi: 10.1017/S0025315407054999 CrossRefGoogle Scholar
  43. Kuczaj SA II, Makecha R, Trone M, Paulos RD, Ramos JAA (2006) Role of peers in cultural innovation and cultural transmission: evidence from the play of dolphin calves. Int J Comp Psychol 19:223–240Google Scholar
  44. Kuczaj SA, Eskelinen HC, Jones BL, Borger-Turner JL (2015a) Gotta go, mom’s calling: dolphin (Tursiops truncatus) mothers use individually distinctive acoustic signals to call their calves. Anim Behav Cogn 2:88–95. doi: 10.12966/abc.02.07.2015 Google Scholar
  45. Kuczaj SA II, Winship KA, Eskelinen HC (2015b) Can bottlenose dolphins (Tursiops truncatus) cooperate when solving a novel task? Anim Cogn 18:543–550. doi: 10.1007/s10071-014-0822-4 CrossRefPubMedGoogle Scholar
  46. Kuczaj SA II, Frick EE, Jones BL, Lea JS, Beecham D, Schnöller F (2015c) Underwater observations of dolphin reactions to a distressed conspecific. Learn Behav 43:289–300. doi: 10.3758/s13420-015-0179-9 CrossRefPubMedGoogle Scholar
  47. Lammers MO, Schotten M, Au WLW (2006) The spatial context of free-rangin Hawaiian spinner dolphins (Stenella longirostris) producing acoustic signals. J Acoust Soc Am 119:1244–1250. doi: 10.1121/1.2151804 CrossRefPubMedGoogle Scholar
  48. Lodi L (1992) Epimeletic behavior of free-ranging rough-toothed dolphins, Steno bredanensis, from Brazil. Mar Mamm Sci 8:284–287. doi: 10.1111/j.1748-7692.1992.tb00410.x CrossRefGoogle Scholar
  49. Lönnstedt OM, Ferrari MCO, Chivers DP (2014) Lionfish predators use flared fin displays to initiate cooperative hunting. Biol Lett 10:1–4. doi: 10.1098/rsbl.2014.0281 CrossRefGoogle Scholar
  50. Mann J, Smuts B (1999) Behavioral development in wild bottlenose dolphin newborns (Tursiops sp.). Behaviour 136:529–566. doi: 10.1163/156853999501469 CrossRefGoogle Scholar
  51. Melis AP, Hare B, Tomasello M (2006) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 72:275–286. doi: 10.1016/j.anbehav.2005.09.018 CrossRefGoogle Scholar
  52. Melis AP, Hare B, Tomasello M (2009) Chimpanzees coordinate in a negotiation game. Evol Hum Behav 30:381–392. doi: 10.1016/j.evolhumbehav.2009.05.003 CrossRefGoogle Scholar
  53. Mello I, Amudin M (2005) Whistle production pre- and post-partum in bottlenose dolphins (Tursiops truncatus) in human care. Aquat Mamm 3:169–175. doi: 10.1578/AM.31.2.2005.169 CrossRefGoogle Scholar
  54. Mendres KA, de Waal FBM (2000) Capuchins do cooperate: the advantages of an intuitive task. Anim Behav 60:523–529. doi: 10.1006/anbe.2000.1512 CrossRefPubMedGoogle Scholar
  55. Möslinger H, Kotrschal K, Huber L, Range F, Virányi Z (2009) Cooperative string-pulling in wolves. J Vet Behav 4:99. doi: 10.1016/j.jveb.2008.09.030 CrossRefGoogle Scholar
  56. Nair S, Balakrishnan R, Seelamantula CS, Sukumar R (2009) Vocalizations of wild Asian elephants (Elephas maximus): structural classification and social context. J Acoust Soc Am 126:2768–2778. doi: 10.1121/1.3224717 CrossRefPubMedGoogle Scholar
  57. Noë R (2006) Cooperation experiments: coordination through communication versus acting apart together. Anim Behav 71:1–18. doi: 10.1016/j.anbehav.2005.03.037 CrossRefGoogle Scholar
  58. Overstrom NA (1983) Association between burst-pulse sounds and aggressive behavior in captive Atlantic bottlenosed dolphins (Tursiops truncatus). Zoo Biol 2:93–103. doi: 10.1002/zoo.1430020203 CrossRefGoogle Scholar
  59. Park KJ, Sohn H, An YR, Moon DY, Choi SG, An DH (2013) An unusual case of care-giving behavior in wild long-beaked common dolphins (Delphinus capensis) in the East Sea. Mar Mamm Sci 29:1–7. doi: 10.1111/mms.12012 CrossRefGoogle Scholar
  60. Péron F, Rat-Fischer L, Lalot M, Nagle L, Bovet D (2011) Cooperative problem solving in African grey parrots (Psittacus erithacus). Anim Cogn 14:545–553. doi: 10.1007/s10071-011-0389-2 CrossRefPubMedGoogle Scholar
  61. Petit O, Desportes C, Thierry B (1992) Differential probability of “coproduction” in two species of macaque (Macaca tonkeana, M. mulatta). Ethology 90:107–120. doi: 10.1111/j.1439-0310.1992.tb00825.x CrossRefGoogle Scholar
  62. Plotnik JM, Lair R, Suphachoksahakun W, de Waal FBM (2011) Elephants know when they need a helping trunk in a cooperative task. Proc Natl Acad Sci USA 108:5116–5121. doi: 10.1073/pnas.1101765108 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Povinelli DJ, O’Neill DK (2000) Do chimpanzees use their gestures to instruct each other? In: Baron-Cohen S, Tager-Flusberg H, Cohen DJ (eds) Understanding other minds: perspectives from developmental cognitive neuroscience. Oxford University Press, Oxford, pp 459–487Google Scholar
  64. Povinelli DJ, Nelson KE, Boysen ST (1992) Comprehension of role reversal in chimpanzees: evidence of empathy? Anim Behav 43:633–640. doi: 10.1016/S0003-3472(05)81022-X CrossRefGoogle Scholar
  65. Quick NJ, Janik VM (2008) Whistle rates of wild bottlenose dolphins (Tursiops truncatus): influences of group size and behavior. J Comp Psychol 122:305–311. doi: 10.1037/0735-7036.122.3.305 CrossRefPubMedGoogle Scholar
  66. Ritter F (2007) Behavioral responses of rough-toothed dolphins to a dead newborn calf. Mar Mamm Sci 23:429–433. doi: 10.1111/j.1748-7692.2007.00107.x CrossRefGoogle Scholar
  67. Sayigh LS, Esch HC, Wells RS, Janik VM (2007) Facts about signature whistles of bottlenose dolphins (Tursiops truncatus). Anim Behav 74:1631–1642. doi: 10.1016/j.anbehav.2007.02.018 CrossRefGoogle Scholar
  68. Seed AM, Clayton NS, Emery N (2008) Cooperative problem solving in rooks (Corvus frugilegus). Proc R Soc B 275:1421–1429. doi: 10.1098/rspb.2008.0111 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Siebenaler JB, Caldwell DK (1956) Cooperation among adult dolphins. J Mamm 37:126–128. doi: 10.2307/1375558 CrossRefGoogle Scholar
  70. Silva-Jr JM, Silva FJL, Sazima I (2005) Rest, nurture, sex, release, and play: diurnal underwater behavior of the spinner dolphin at Fernando de Noronha Archipelago, SW Atlantic. J Ichthyol Aquat Biol 9(4):161–176Google Scholar
  71. Simões-Lopes PC, Fabian ME, Menegheti JO (1998) Dolphin interaction with the mullet artisanal fishing on southern Brazil: a qualitative and quantitative approach. Rev Bras Zool 15:709–726. doi: 10.1590/S0101-81751998000300016 CrossRefGoogle Scholar
  72. Smith BD, Tun MT, Chit AM, Win H, Moe T (2009) Catch composition and conservation management of a human-dolphin cooperative cast-net fishery in the Ayeyarwady river, Myanmar. Biol Conserv 142:1042–1049. doi: 10.1016/j.biocon.2009.01.015 CrossRefGoogle Scholar
  73. Smolker RA, Pepper JW (1999) Whistle convergence among allied male bottlenose dolphins (Delphinidae, Tursiops sp.). Ethology 105:595–617. doi: 10.1046/j.1439-0310.1999.00441.x CrossRefGoogle Scholar
  74. Steiner WW, Hain JH, Winn HE, Perkins PJ (1979) Vocalizations and feeding behavior of the killer whale (Orcinus orca). J Mamm 60:823–827. doi: 10.2307/1380199 CrossRefGoogle Scholar
  75. Tavolga MC (1966) Behavior of the bottlenose dolphin (Tursiops truncatus): social interactions in a captive colony. In: Norris KS (ed) Whales, dolphins, and porpoises. University of California Press, Berkeley, pp 718–730Google Scholar
  76. Tebbich S, Taborsky M, Winkler H (1996) Social manipulation causes cooperation in keas. Anim Behav 52:1–10. doi: 10.1006/anbe.1996.0147 CrossRefGoogle Scholar
  77. Torres LG, Read AJ (2009) Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida. Mar Mamm Sci 25:797–815. doi: 10.1111/j.1748-7692.2009.00297.x CrossRefGoogle Scholar
  78. Tyack P (1986) Whistle repertoires of two bottlenosed dolphins, Tursiops truncatus: mimicry of signature whistles? Behav Ecol Sociobiol 18:251–2577. doi: 10.1007/bf00300001 CrossRefGoogle Scholar
  79. Tyack PL (1997) Development and social functions of signature whistles in bottlenose dolphins Tursiops truncatus. Bioacoustics 8:21–46. doi: 10.1080/09524622.1997.9753352 CrossRefGoogle Scholar
  80. Vaughn RL, Shelton DE, Timm LL, Watson LA, Würsig B (2007) Dusky dolphin (Lagenorhynchus obscurus) feeding tactics and multi-species associations. N Z J Mar Freshwater Res 41:391–400. doi: 10.1080/00288330709509929 CrossRefGoogle Scholar
  81. Visser IN, Smith TG, Bullock ID, Green GD, Carlsson OG, Imberti S (2008) Antarctic peninsula killer whales (Orcinus orca) hunt seals and a penguin on floating ice. Mar Mamm Sci 24:225–234. doi: 10.1111/j.1748-7692.2007.00163.x CrossRefGoogle Scholar
  82. Warneken F, Chen F, Tomasello M (2006) Cooperative activities in young children and chimpanzees. Child Dev 77:640–663. doi: 10.1111/j.1467-8624.2006.00895.x CrossRefPubMedGoogle Scholar
  83. Warren-Smith AB, Dunn WL (2006) Epimeletic behaviour toward a seriously injured juvenile bottlenose dolphin (Tursiops sp.) in port phillip, Victoria, Australia. Aquat Mamm 32:357–362. doi: 10.1578/AM.32.3.2006.357 CrossRefGoogle Scholar
  84. Watwood SL, Tyack PL, Wells RS (2004) Whistle sharing in paired male bottlenose dolphins, Tursiops truncatus. Behav Ecol Sociobiol 55:531–543. doi: 10.1007/s00265-003-0724-y CrossRefGoogle Scholar
  85. Wells RS (1991) The role of long-term study in understanding the social structure of a bottlenose dolphin community. In: Pryor K, Norris KS (eds) Dolphin societies: discoveries and puzzles. University of California Press, Berkley, pp 199–225Google Scholar
  86. Würsig B, Würsig M (1980) Behavior and ecology of the dusky dolphin, Lagenorhynchus obscurus, in the south Atlantic. Fish Bull 77:399–412Google Scholar
  87. Xitco MJ, Gory JD, Kuczaj SA (2001) Spontaneous pointing by bottlenose dolphins (Tursiops truncatus). Anim Cogn 4:115–123. doi: 10.1007/s100710100107 CrossRefGoogle Scholar
  88. Yamamoto S, Tanaka M (2009) Do chimpanzees (Pan troglodytes) spontaneously take turns in a reciprocal cooperation task? J Comp Psychol 123:242–249. doi: 10.1037/a0015838 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Dolphins Plus, Inc.Key LargoUSA
  2. 2.University of Southern MississippiHattiesburgUSA

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