Visible and invisible displacement with dynamic visual occlusion in bottlenose dolphins (Tursiops spp)

Abstract

Anticipating the location of a temporarily obscured target—what Piaget (the construction of reality in the child. Basic Books, New York, 1954) called “object permanence”—is a critical skill, especially in hunters of mobile prey. Previous research with bottlenose dolphins found they could predict the location of a target that had been visibly displaced into an opaque container, but not one that was first placed in an opaque container and then invisibly displaced to another container. We tested whether, by altering the task to involve occlusion rather than containment, these animals could show more advanced object permanence skills. We projected dynamic visual displays at an underwater-viewing window and videotaped the animals’ head moves while observing these displays. In Experiment 1, the animals observed a small black disk moving behind occluders that shifted in size, ultimately forming one large occluder. Nine out of ten subjects “tracked” the presumed movement of the disk behind this occluder on their first trial—and in a statistically significant number of subsequent trials—confirming their visible displacement abilities. In Experiment 2, we tested their invisible displacement abilities. The disk first disappeared behind a pair of moving occluders, which then moved behind a stationary occluder. The moving occluders then reappeared and separated, revealing that the disk was no longer behind them. The subjects subsequently looked to the correct stationary occluder on eight of their ten first trials, and in a statistically significant number of subsequent trials. Thus, by altering the stimuli to be more ecologically valid, we were able to show that the dolphins could indeed succeed at an invisible displacement task.

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References

  1. Aguiar A, Baillargeon R (2002) Developments in young infants reasoning about occluded objects. Cogn Psychol 45:267–336

    PubMed Central  PubMed  Article  Google Scholar 

  2. Au WWL (1993) The sonar of dolphins. Springer, New York

    Book  Google Scholar 

  3. Bräuer J, Kaminski J, Riedel J, Call J, Tomasello M (2006) Making inferences about the location of hidden food: social dog, causal ape. J Comp Psychol 120:38–47

    PubMed  Article  Google Scholar 

  4. Bugnyar T, Stowe M, Henrich B (2007) The ontogeny of caching in ravens, Corvus corax. Anim Behav 74:757–767

    Article  Google Scholar 

  5. Call J (2001) Object permanence in orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes) and children (Homo sapiens). J Comp Psychol 155:159–171

    Article  Google Scholar 

  6. Chevalier-Skolnikoff S, Poirier FE (1977) Primate biosocial development. Garland, New York

    Google Scholar 

  7. Collier-Baker E, Davis JM, Suddendorf T (2004) Do dogs (Canis familiaris) understand invisible displacement? J Comp Psychol 118:421–433

    PubMed  Article  Google Scholar 

  8. Collier-Baker E, Davis JM, Nielsen M, Suddendorf T (2006) Do chimpanzees (Pan troglodytes) understand invisible displacement? Anim Cogn 9:55–61

    PubMed  Article  Google Scholar 

  9. Dawson WW (1980) The cetacean eye. In: Herman LM (ed) Cetacean behavior: mechanisms and functions. Wiley, New York, pp 53–100

    Google Scholar 

  10. De Blois ST, Novack MA (1994) Object permanence in rhesus monkeys (Macaca mulatta). J Comp Psychol 108:318–327

    Article  Google Scholar 

  11. De Blois ST, Novack MA, Bond M (1998) Object permanence in orangutans (Pongo pygmaeus) and squirrel monkeys (Saimiri sciuereus). J Comp Psychol 112:137–152

    PubMed  Article  Google Scholar 

  12. De Blois ST, Novack MA, Bond M (1999) Can memory requirements account for species differences in invisible displacement tasks? J Exp Psychol Anim Behav Process 25:168–176

    PubMed  Article  Google Scholar 

  13. Doré FY, Dumas C (1987) Psychology of animal cognition: Piagetian studies. Psychol Bull 107:219–223

    Article  Google Scholar 

  14. Doré FY, Goulet S (1998) The comparative analysis of object knowledge. In: Langer J, Killen L (eds) Piaget, evolution and development. Erlbaum, Mahwah, pp 55–72

    Google Scholar 

  15. Doré FY, Fiset S, Goulet S, Dumas MC, Gagnon S (1996) Search behavior in cats and dogs: interspecific differences in working memory and spatial cognition. Anim Learn Behav 24:142–149

    Article  Google Scholar 

  16. Dumas C (1992) Object permanence in cats (Felis catus): an ecological approach to the study of invisible displacements. J Comp Psychol 106:404–410

    CAS  PubMed  Article  Google Scholar 

  17. Dumas C, Wilke DW (1995) Object permanence in ring doves (Streptopelia risoria). J Comp Psychol 2:142–150

    Article  Google Scholar 

  18. Fiset S, Le Blanc V (2007) Invisible displacement understanding in domestic dogs (Canis familiaris): the role of visual cues in search behavior. Anim Cogn 10:211–224

    PubMed  Article  Google Scholar 

  19. Funk MS (1996) Development of object permanence in the New Zealand parakeet (Cyanoramphus auriceps). Anim Learn Behav 24:375–383

    Article  Google Scholar 

  20. Goulet S, Doré FY, Rosseau R (1994) Object permanence and working memory in cats (Felis catus). J Exp Psychol Anim Behav Process 20:347–365

    CAS  PubMed  Article  Google Scholar 

  21. Greene W, Melillo-Sweeting K, Dudzinski KM (2011) Comparing object play in captive and wild dolphins. Int J Comp Psychol 24:292–306

    Google Scholar 

  22. Harley HE (2013) Consciousness in dolphins? A review of recent evidence. J Comp Physiol A 199:565–582

    Article  Google Scholar 

  23. Harley HE, Roitblat HL, Nachtigall PE (1996) Object representation in the bottlenose dolphin (Tursiops truncatus): integration of visual and echoic information. J Exp Psychol Anim Behav Process 22:164–174

    CAS  PubMed  Article  Google Scholar 

  24. Hauser MD (2001) Searching for food in the wild: a nonhuman primate’s expectation about invisible displacement. Dev Sci 4:84–93

    Article  Google Scholar 

  25. Herman LM (1991) What the dolphin knows, or might know, about its natural world. In: Pryor K, Norris KS (eds) Dolphin societies: discoveries and puzzles. University of California Press, Berkeley, pp 349–361

    Google Scholar 

  26. Herman LM (2002) Vocal, social, and self-imitation by bottlenosed dolphins. In: Dautenhahn K, Nehaniv C (eds) Imitation in animals and artifacts. MIT Press, Cambridge, pp 63–108

    Google Scholar 

  27. Herman LM (2006) Intelligence and rational behavior in the bottlenosed dolphin. In: Hurley S, Nudds M (eds) Rational animals?. Oxford University Press, Oxford, pp 439–467

    Chapter  Google Scholar 

  28. Herman LM, Forestell PH (1985) Reporting presence or absence of named objects by a language-trained dolphin. Neurosci Biobehav R 9:667–681

    CAS  Article  Google Scholar 

  29. Herman LM, Hovancik JR, Gory JD, Bradshaw GL (1989) Generalizations of visual matching by a bottlenosed dolphin (Tursiops truncatus): evidence for invariance of cognitive performance with visual or auditory materials. J Exp Psychol Anim Behav Process 15:124–136

    Article  Google Scholar 

  30. Herman LM, Morrel-Samuels P, Pack AA (1990) Bottlenosed dolphin and human recognition of veridical and degraded video displays of an artificial gestural language. J Exp Psychol Gen 119:215–230

    CAS  PubMed  Article  Google Scholar 

  31. Herman LM, Pack AA, Morrel-Samuels P (1993) Representational and conceptual skills of dolphins. In: Roitblat RH, Herman LM, Nachtigall P (eds) Language and communication: comparative perspectives. Erlbaum, Hillsdale, pp 273–298

    Google Scholar 

  32. Herman LM, Pack AA, Hoffman-Kuhnt M (1998) Seeing through sound: dolphins (Tursiops truncatus) perceive spatial structure of objects through echolocation. J Comp Psychol 112:292–305

    CAS  PubMed  Article  Google Scholar 

  33. Hespos SJ, Baillargeon R (2001) Infants’ knowledge about occlusion and containment events: a surprising discrepancy. Psychol Sci 12:141–147

    CAS  PubMed  Article  Google Scholar 

  34. Jaakkola K, Guarino E, Rodriguez M, Erb L, Trone M (2010) What do dolphins (Tursiops truncatus) understand about hidden objects? Anim Cogn 13:103–120  

  35. Johnson CM (2010) Observing cognitive complexity in primates and cetaceans. Int J Comp Psychol 23:587–624

    Google Scholar 

  36. Kuczaj SA, Trone M (2001) Why do dolphins and whales make their play more difficult? Genet Epistemol 29:57

    Google Scholar 

  37. Kuczaj SA, Walker RT (2006) How do dolphins solve problems? In: Wasserman EA, Zentall TR (eds) Comparative cognition: experimental explorations of animal intelligence. Oxford University Press, Oxford, pp 580–600

    Google Scholar 

  38. Kuczaj SA, Yeater DB (2006) Dolphin imitation: who, what, when and why? Aquat Mamm 32:413–422

    Article  Google Scholar 

  39. Leslie AM (1987) Pretense and representation in finance: the origins of “theory of mind”. Psychol Rev 94:412–426

    Article  Google Scholar 

  40. Madsen CJ, Herman LM (1980) Social and ecological correlates of cetacean vision and visual appearance. In: Herman LM (ed) Cetacean behavior: mechanisms and functions. Wiley, New York, pp 101–148

    Google Scholar 

  41. Marino L, Connor RC, Fordyce RE, Herman LM, Hof PR, Lefebvre L, Whitehead H (2007) Cetaceans have complex brains for complex cognition. PLoS Biol 5:0966–0972

    CAS  Article  Google Scholar 

  42. McCowan B, Marino L, Vance E, Walker L, Reiss D (2000) Bubble ring play of bottlenose dolphins (Tursiops truncatus): implications for cognition. J Comp Psychol 114:98–106

    CAS  PubMed  Article  Google Scholar 

  43. Mitchell RW, Hoban E (2010) Does echolocation make understanding object permanence unnecessary? Failure to find object permanence understanding in dolphins and beluga whales. In: Dolins FL, Mitchell RW (eds) Spatial cognition, spatial perception: mapping the self and space. Cambridge University Press, Cambridge, pp 258–280

    Google Scholar 

  44. Neiworth JJ, Steinmark E, Basile BM, Wonders R, Steely F, de Hart C (2003) A test of object permanence in a new-world monkey species, cotton top tamarins (Saguinus oedipus). Anim Cogn. doi:10.1007/s10071-003-0162-2

    PubMed  Google Scholar 

  45. Pace DS (2000) Fluke-made bubble rings as toys in bottlenose dolphin calves (Tursiops truncatus). Aquat Mamm 26:57–64

    Google Scholar 

  46. Pack AA, Herman LM (1995) Sensory integration and the bottlenosed dolphin: immediate recognition of complex shapes across the senses of echolocation and vision. J Acoust Soc Am 98:722–733

    CAS  PubMed  Article  Google Scholar 

  47. Pepperberg IM (2002) The value of the Piagetian framework for comparative cognitive studies. Anim Cogn 5:177–182

    PubMed  Article  Google Scholar 

  48. Pepperberg IM, Funk MS (1990) Object permanence in four species of psittacine birds: an African grey parrot (Psittacus erithacus), an Illiger mini macaw (Ara maracana), a parakeet (Melopsittacus undulatus) and a cockatiel (Nymphicus hollandicus). Anim Learn Behav 18:97–108

    Article  Google Scholar 

  49. Perner J (1991) Understanding the representational mind. MIT Press, Cambridge

    Google Scholar 

  50. Piaget J (1954) The construction of reality in the child. Basic Books, New York

    Book  Google Scholar 

  51. Piaget J (1974) Biology and knowledge. University of Chicago Press, Chicago

    Google Scholar 

  52. Pollock B, Prior H, Güntürkün O (2000) Development of object permanence in food-storing magpies (Pica pica). J Comp Psychol 114:148–157

    Article  Google Scholar 

  53. Pryor K, Haag R, O’Reilly J (1969) The creative porpoise: training for novel behavior. J Exp Anal Behav 12:653–661

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  54. Reiss D, Marino L (2001) Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proc Natl Acad Sci USA 98:5937–5942

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  55. Rendell L, Whitehead H (2001) Culture in whales and dolphins. Behav Brain Sci 24:309–382

    CAS  PubMed  Article  Google Scholar 

  56. Ridgway SH (1990) The central nervous system of the bottlenose dolphin. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, New York, pp 69–97

    Chapter  Google Scholar 

  57. Roitblat HL, Au WWL, Nachtigall PE, Shizumura R, Moons G (1995) Sonar recognition of targets embedded in sediment. Neural Netw 8:1263–1273

    Article  Google Scholar 

  58. Rooijakkers EF, Kaminski J, Call J (2009) Comparing dogs and great apes in their ability to visually track object transpositions. Anim Cogn. doi:10.1007/s10071-009-0238-8

    PubMed Central  PubMed  Google Scholar 

  59. Rossbach KA, Herzing DL (1997) Underwater observations of benthic-feeding bottlenose dolphins (Tursiops truncatus) near Grand Bahama Island, Bahamas. Mar Mamm Sci 13:498–504

    Article  Google Scholar 

  60. Shepard R (1994) Perceptual–cognitive universals as reflections of the world. Psychon Bull Rev 1:2–28

    CAS  PubMed  Article  Google Scholar 

  61. Shettleworth SJ (1998) Cognition, evolution and behavior. Oxford University Press, Oxford

    Google Scholar 

  62. Suddendorf T, Whiten A (2001) Mental evolution and development: evidence for secondary representations in children, great apes, and other animals. Psychol Bull 127:629–650

    CAS  PubMed  Article  Google Scholar 

  63. Tavolga CM (1966) Behavior of the bottlenosed dolphin (Tursiops truncatus): Social interactions in a captive colony. In: Norris KS (ed) Whales, dolphins and porpoises. University of California Press, Los Angeles, pp 718–730

    Google Scholar 

  64. Taylor CK, Saayman GS (1973) Imitative behaviour by Indian Ocean bottlenose dolphins (Tursiops aduncus) in captivity. Behaviour 44:286–298

    Article  Google Scholar 

  65. Thomas JA, Kastelein RA (1990) Sensory abilities of cetaceans. Plenum Press, New York

    Book  Google Scholar 

  66. Zucca P, Milos N, Vallortigara G (2006) Piagetian object permanence and its development in Eurasian jays (Garrulus glandarius). Anim Cogn. doi:10.1007/s10071-006-0063-2

    Google Scholar 

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Acknowledgments

We are indebted to Sea World, San Diego, for allowing us access to the animals, and especially to Dr. Judy St. Leger, DVM, and to Scott Collins, Brittany Harris and the rest of the Animal Care Staff at Rocky Point Preserve, for their support and encouragement. Special thanks to Whitney Friedman and Adam Tinkle who served as observers on this project, and to two anonymous reviewers for helpful suggestions regarding our analyses and text. This research was funded in part by a Jacobs Fellowship and an NSF GRFP to JS.

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Correspondence to Christine M. Johnson.

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Johnson, C.M., Sullivan, J., Buck, C.L. et al. Visible and invisible displacement with dynamic visual occlusion in bottlenose dolphins (Tursiops spp). Anim Cogn 18, 179–193 (2015). https://doi.org/10.1007/s10071-014-0788-2

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Keywords

  • Object permanence
  • Invisible displacement
  • Bottlenose dolphins
  • Occlusion
  • Secondary representations