Animal Cognition

, Volume 19, Issue 6, pp 1133–1142 | Cite as

Harbour seals (Phoca vitulina) are able to time precisely

  • Tamara Heinrich
  • Guido Dehnhardt
  • Frederike D. HankeEmail author
Original Paper


Time along with space is one of the two fundamental dimensions of life. Whereas spatial aspects have been considered in experiments with marine mammals, research has so far not focused on timing per se although it is most likely involved in many behaviours such as foraging or navigation. This study investigated whether harbour seals possess a sense of time and how precisely they are able to discriminate time intervals. Experiments took place in a chamber that allowed keeping ambient illumination constant at 40 lx. The animal was presented with a white circle on a black background on a monitor displayed for a preset time interval. In a two-alternative forced-choice experiment, the animal had to indicate the presence of the standard or a longer comparison time interval by moving its head to one out of two response targets. Time difference thresholds were assessed for various standard intervals between 3 to 30 s adopting a staircase procedure. The experimental animal found access to the task easily and discriminated time intervals with difference thresholds partly in the millisecond range. Thus our study revealed a well-developed sense of time in a pinniped species. Time, besides information provided by the classical senses, is thus most likely an important parameter seals can rely on for various tasks including navigation and foraging.


Timing Interval timing Pinnipeds Sense of time Time difference thresholds 



The authors would like to express their sincere thanks to Lars Miersch for technical assistance and to all colleagues at the Marine Science Center for ideas and support.


This study was supported by a grant of the VolkswagenStiftung to GD and a grant of the Landesgraduiertenfoerderung Mecklenburg-Vorpommern to TH.

Complaince with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The experiments were carried out in accordance with the European Communities Council Directive of November 24, 1986 (86/609/EEC). According to § 8 of the German Animal Welfare Act of May 18, 2006 (BGB I. I S. 1206, 1313), experiments conducted in this study were not subject to approval or notification, since they did not cause pain, suffering or injuries to the animals.


  1. Bateson M, Kacelnik A (1997) A starling’s preferences for predictable and unpredictable delays to food. Anim Behav 53:1129–1142CrossRefPubMedGoogle Scholar
  2. Boisvert MJ, Sherry DF (2006) Interval timing by an invertebrate, the bumble bee Bombus impatiens. Curr Biol 16:1636–1640CrossRefPubMedGoogle Scholar
  3. Bowen WD, Boness DJ, Iverson SJ (1999) Diving behaviour of lactating harbour seals and their pups during maternal foraging trips. Can J Zool 77:978–988CrossRefGoogle Scholar
  4. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436CrossRefPubMedGoogle Scholar
  5. Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nature Neurosci 6:755–765CrossRefGoogle Scholar
  6. Buhusi CV, Sasaki A, Meck WH (2002) Temporal integration as a function of signal and gap intensity in rats (Rattus norvegicus) and pigeons (Coumbia livia). J Comp Psychol 116:381–390CrossRefPubMedGoogle Scholar
  7. Buhusi CV, Perera D, Meck WH (2005) Memory for timing visual and auditory signals in albino and pigmented rats. J Exp Psychol Anim Behav Proc 31:18–30CrossRefGoogle Scholar
  8. Cheng K, Roberts WA (1991) Three pyschophysical principles of timing in pigeons. Learn Motiv 22:112–128CrossRefGoogle Scholar
  9. Chouhan NS, Wolf R, Helfrich-Förster C, Heisenberg M (2015) Flies remember the time of day. Curr Biol 25:1619–1624CrossRefPubMedGoogle Scholar
  10. Church RM (1984) Properties of the internal clock. Ann NY Acad Sci 423:566–582CrossRefPubMedGoogle Scholar
  11. Church RM, Getty DJ, Lerner ND (1976) Duration discrimination by rats. J Exp Psychol Anim Behav Proc 2:303–312CrossRefGoogle Scholar
  12. Cook P, Rouse A, Wilson MA, Reichmuth C (2013) A California sea lion (Zalophus californianus) can keep the beat: motor entrainment to rhythmic auditory stimuli in a non vocal mimic. J Comp Psychol 127:412–427CrossRefPubMedGoogle Scholar
  13. Cornick LA, Horning M (2003) A test of hypotheses based on optimal foraging considerations for a diving mammal using a novel experimental approach. Can J Zool 81:1799–1807CrossRefGoogle Scholar
  14. Crystal JD (2001) Nonlinear time perception. Behav Process 55:35–49CrossRefGoogle Scholar
  15. Dehnhardt G, Kaminski A (1995) Sensitivity of the mystacial vibrissae of harbour seals (Phoca vitulina) for size differences of actively touched objects. J Exp Biol 198:2317–2323PubMedGoogle Scholar
  16. Dehnhardt G, Mauck B (2008) Mechanoreception in secondarily aquatic vertebrates. In: Thewissen JGW, Nummela S (eds) Sensory evolution on the threshold, adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 295–314Google Scholar
  17. Dews PB (1978) Studies on responding under fixed-interval schedules of reinforcement: II. The scalloped pattern of the cumulative record. J Exp Anal Behav 29:67–75CrossRefPubMedPubMedCentralGoogle Scholar
  18. Drew MR, Zupan B, Cooke A, Couvillon PA, Balsam PD (2005) Temporal control of conditioned responding in goldfish. J Exp Psychol Anim Behav Proc 31:31–39CrossRefGoogle Scholar
  19. Droit-Volet S (2013) Time perception in children: a neurodevelopmental approach. Neuropsychologia 51:220–234CrossRefPubMedGoogle Scholar
  20. Ehrenstein WH, Ehrenstein A (1999) Modern techniques in neuroscience research. In: Windhorst U, Johansson H (eds) Psychophysical methods. Springer Verlag, Berlin, pp 1211–1241Google Scholar
  21. Etienne AS, Jeffrey KJ (2004) Path integration in mammals. Hippocampus 14:180–192CrossRefPubMedGoogle Scholar
  22. Fetterman JG, Killeen PR (1991) Adjusting the pacemaker. Learn Motiv 22:226–252CrossRefGoogle Scholar
  23. Fetterman JG, Killeen PR (1992) Time discrimination in Columbia livia and Homo sapiens. J Exp Psychol 18:80–94Google Scholar
  24. Gallistel CR (1990) The organization of learning. MIT Press, CambridgeGoogle Scholar
  25. Gallistel CR, King A, McDonald R (2004) Sources of variability and systematic error in mouse timing behavior. J Exp Psychol Anim Behav Proc 30:3–16CrossRefGoogle Scholar
  26. Gellermann LW (1933) Chance orders of alternating stimuli in visual discrimination experiments. J Genet Psychol 42:206–208Google Scholar
  27. Gescheider GA (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, New YorkGoogle Scholar
  28. Gibbon J (1977) Scalar expectancy theory and Weber’s law in animal timing. Psychol Rev 84:279–325CrossRefGoogle Scholar
  29. Gibbon J (1991) Origins of scalar timing. Learn Motiv 22:3–38CrossRefGoogle Scholar
  30. Gibbon J, Church RM, Meck WH (1984) Scalar timing in memory. Ann NY Acad Sci 423:52–77CrossRefPubMedGoogle Scholar
  31. Gibbon J, Malapani C, Dale CL, Gallistel CR (1997) Toward a neurobiology of temporal cognition: advances and challenges. Curr Opin Neurobiol 7:170–184CrossRefPubMedGoogle Scholar
  32. Gläser N, Mauck B, Kandil F, Lappe M, Dehnhardt G, Hanke FD (2014) Harbour seals (Phoca vitulina) can perceive optic flow underwater. PLoS One 9:e103555CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gribova A, Donchin O, Bergman H, Vaadia E, Cadoso de Oliveira S (2002) Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area. Exp Brain Res 146:322–335CrossRefPubMedGoogle Scholar
  34. Grondin S (2001) From physical time to the first and second moments of psychological time. Psychol Bull 127(1):22–44CrossRefPubMedGoogle Scholar
  35. Grondin S (2010) Timing and time perception: a review of recent behavioral and neuroscience findings and theoretical directions. Atten Percept Psychophys 72:561–582CrossRefPubMedGoogle Scholar
  36. Grondin S (2012) Violation of the scalar property for time perception between 1 and 2 seconds: evidence from interval discrimination, reproduction, and categorization. J Exp Psychol Human 38:880–890CrossRefGoogle Scholar
  37. Grondin S (2014) About the (non)scalar property for time perception. In: Merchant H, de Lafuente V (eds) Neurobiology of interval timing. Springer, New York, pp 17–32Google Scholar
  38. Grondin S, Killeen PR (2009) Tracking time with song and count: different Weber functions for musicians and nonmusicians. Atten Percept Psychophys 71:1649–1654CrossRefPubMedGoogle Scholar
  39. Hanke FD, Miersch L, Warrant EJ, Mitschke FM, Dehnhardt G (2013) Are harbour seals (Phoca vitulina) able to perceive and use polarised light? J Comp Physiol A 199:509–519CrossRefGoogle Scholar
  40. Heaslip SG, Bowen WD, Iverson SJ (2014) Testing predictions of optimal diving theory using animal-borne video from harbour seals (Phoca vitulina concolor). Can J Zool 92:309–318CrossRefGoogle Scholar
  41. Higa JJ, Simm LA (2004) Interval timing in Siamese fighting fish (Betta splendens). Behav Process 67:501–509CrossRefGoogle Scholar
  42. Huang J-S, Shimomura Y, Katsuura T (2012) Effects of monochromatic light on different time perception. J Hum Environ Syst 15:21–29CrossRefGoogle Scholar
  43. Katsuura T, Yasuda T, Shimomura Y, Iwanaga K (2007) Effects of monochromatic light on time sense for short intervals. J Physiol Anthropol 26:95–100CrossRefPubMedGoogle Scholar
  44. Kleiner M, Brainard DH, Pelli DG (2007) What’s new in Psychtoolbox-3? Perception 36 (ECVP Abstract Supplement)Google Scholar
  45. Krebs JR, Davies NB (1981) An introduction to behavioral ecology. Blackwell Scientifiy Publishing, OxfordGoogle Scholar
  46. Kuriyama K et al (2003) Circadian fluctuation of time perception in healthy human subjects. Neurosci Res 46:23–31CrossRefPubMedGoogle Scholar
  47. Kuriyama K et al (2005) Diurnal fluctuation of time perception under 30-h sustained wakefulness. Neurosci Res 53:123–128CrossRefPubMedGoogle Scholar
  48. Lejeune H, Wearden JH (1991) The comparative psychology of fixed-interval responding: some quantitative analyses. Learn Motiv 22:84–111CrossRefGoogle Scholar
  49. Lejeune H, Wearden JH (2006) Scalar properties in animal timing: conformity and violations. Q J Exp Psychol 59:1875–1908CrossRefGoogle Scholar
  50. Lesage V, Hammil MO, Kovacs KM (1999) Functional classification of harbor seal (Phoca vitulina) dives using depth profiles, swimming velocity, and an index of foraging success. Can J Zool 77:74–87CrossRefGoogle Scholar
  51. Maaß E (2015) Orientation in harbor seals (Phoca vitulina) – can harbor seals reproduce distances?. University of Rostock, GermanyGoogle Scholar
  52. Matell MS, Meck WH (2000) Neuropsychological mechanisms of interval timing behavior. BioEssays 22:94–103CrossRefPubMedGoogle Scholar
  53. Merchant H, de Lafuente V (2014) Introduction to the neurobiology of interval timing. In: Merchant H, de Lafuente V (eds) Neurobiology of interval timing. Springer, New York, pp 1–13Google Scholar
  54. Mittelstaedt H, Mittelstaedt M-L (1982) Homing by path integration. In: Papi F, Wallraff HG (eds) Avian Navigation - International Symposium on Avian Navigation (ISAN) held at Tirrenia (Pisa), September 11-14, 1981. Springer, Berlin, pp 290–298Google Scholar
  55. Mori Y (1998) The optimal patch use in divers: optimal time budget and the number of dive cycles druing bout. J Theor Biol 190:187–199CrossRefGoogle Scholar
  56. Morita T, Fukui T, Morofushi M, Tokura H (2007) Subjective time runs faster under the influence of bright rather than dim light conditions during the forenoon. Physiol Behav 91:42–45CrossRefPubMedGoogle Scholar
  57. Ohyama T, Gibbon J, Deich JD, Balsam PD (1999) Temporal control during maintenance and extinction of conditioned keypecking in ring doves. Anim Learn Behav 27:89–98CrossRefGoogle Scholar
  58. Papi F (ed) (1992) Animal homing. Animal Behaviour Series, Chapman and HallGoogle Scholar
  59. Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437–442CrossRefPubMedGoogle Scholar
  60. Penney TB, Gibbon J, Meck WH (2008) Categorical scaling of duration bisection in pigeons (Columba livia), mice (Mus musculus), and humans (Homo sapiens). Psychol Sci 19:1103–1109CrossRefPubMedGoogle Scholar
  61. Rakitin BC, Gibbon J, Penney TB, Malapani C, Hinten SC, Meck WH (1996) Scalar expectancy theory and peak-interval timing in humans. J Exp Psychol Anim Behav Proc 24:15–33CrossRefGoogle Scholar
  62. Ramasco V, Biuw M, Nilssen KT (2014) Improving time budget estimates through the behavioural interpretation of dive bouts in harbour seals. Anim Behav 94:117–134CrossRefGoogle Scholar
  63. Richelle M, Lejeune H (1984) Timing competence and timing performance: a cross-species approach. Ann NY Acad Sci 523:254–268CrossRefGoogle Scholar
  64. Ries EH, Traut IM, Paffen P, Goedhart PW (1997) Diving patterns of harbour seals (Phoca vitulina) in the Wadden Sea, the Netherlands and Germany, as indicated by VHF telemetry. Can J Zool 75:2063–2068CrossRefGoogle Scholar
  65. Rosenkilde CE, Divac I (1976) Discrimination of time intervals in cats. Acta Neurobiologica 36:311–317Google Scholar
  66. Rouse A, Cook P, Large EW, Reichmuth C (2016) Beat keeping in a sea lion as coupled oscillation: implications for comparative understanding of human rhythm. Front Neurosci 10:257CrossRefPubMedPubMedCentralGoogle Scholar
  67. Scholtyssek C, Kelber A, Dehnhardt G (2008) Brightness discrimination in the harbor seal (Phoca vitulina). Vis Res 48:96–103CrossRefPubMedGoogle Scholar
  68. Scholtyssek C, Kelber A, Hanke FD, Dehnhardt G (2013) Same different concept formation in a harbor seal (Phoca vitulina). Anim Cogn 16:915–925CrossRefPubMedGoogle Scholar
  69. Scholtyssek C, Kelber A, Dehnhardt G (2015) Why do seals have cones? Behavioral evidence for colorblindness in harbor seals. Anim Cogn 18:551–560CrossRefPubMedGoogle Scholar
  70. Sparling CE, Georges J-Y, Gallon SL, Fedak M, Thompson D (2007) How long does a dive last? Foraging decisions by breath-hold divers in a patchy environment: a test of a simple model. Anim Behav 74:207–218CrossRefGoogle Scholar
  71. Stubbs A (1968) The discrimination of stimulus durations by pigeons. J Exp Anal Behav 11:225–238CrossRefGoogle Scholar
  72. Thompson D, Fedak MA (2001) How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim Behav 61:287–296CrossRefGoogle Scholar
  73. Thompson PM, Miller D (1990) Summer foraging activity and movements of radio-tagged common seals (Phoca vitulina) in the Moray Firth, Scotland. J Appl Ecol 27:492–501CrossRefGoogle Scholar
  74. Treisman M (1963) Temporal discrimination and the indifference interval: implications for a model of the “internal clock”. Psychol Monogr Gen A 77:1–31CrossRefGoogle Scholar
  75. Wearden JH (1991) Do humans possess an internal clock with scalar timing properties? Learn Mem 22:59–83Google Scholar
  76. Wieskotten S, Mauck B, Miersch L, Dehnhardt G, Hanke W (2011) Hydrodynamic discrimination of wakes caused by objects of different size or shape in a harbour seal (Phoca vitulina). J Exp Biol 214:1922–1930CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Tamara Heinrich
    • 1
  • Guido Dehnhardt
    • 1
  • Frederike D. Hanke
    • 1
    Email author
  1. 1.Institute for Biosciences, Sensory and Cognitive EcologyUniversity of RostockRostockGermany

Personalised recommendations