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Harbour seals (Phoca vitulina) are able to time precisely

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Abstract

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.

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References

  • Bateson M, Kacelnik A (1997) A starling’s preferences for predictable and unpredictable delays to food. Anim Behav 53:1129–1142

    Article  CAS  PubMed  Google Scholar 

  • Boisvert MJ, Sherry DF (2006) Interval timing by an invertebrate, the bumble bee Bombus impatiens. Curr Biol 16:1636–1640

    Article  CAS  PubMed  Google Scholar 

  • Bowen WD, Boness DJ, Iverson SJ (1999) Diving behaviour of lactating harbour seals and their pups during maternal foraging trips. Can J Zool 77:978–988

    Article  Google Scholar 

  • Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436

    Article  CAS  PubMed  Google Scholar 

  • Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nature Neurosci 6:755–765

    Article  CAS  Google Scholar 

  • 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 116:381–390

    Article  PubMed  Google Scholar 

  • 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 31:18–30

    Article  Google Scholar 

  • Cheng K, Roberts WA (1991) Three pyschophysical principles of timing in pigeons. Learn Motiv 22:112–128

    Article  Google Scholar 

  • Chouhan NS, Wolf R, Helfrich-Förster C, Heisenberg M (2015) Flies remember the time of day. Curr Biol 25:1619–1624

    Article  CAS  PubMed  Google Scholar 

  • Church RM (1984) Properties of the internal clock. Ann NY Acad Sci 423:566–582

    Article  CAS  PubMed  Google Scholar 

  • Church RM, Getty DJ, Lerner ND (1976) Duration discrimination by rats. J Exp Psychol Anim Behav Proc 2:303–312

    Article  CAS  Google Scholar 

  • 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 127:412–427

    Article  PubMed  Google Scholar 

  • 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 81:1799–1807

    Article  Google Scholar 

  • Crystal JD (2001) Nonlinear time perception. Behav Process 55:35–49

    Article  Google Scholar 

  • 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 198:2317–2323

    CAS  PubMed  Google Scholar 

  • 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 295–314

    Google Scholar 

  • Dews PB (1978) Studies on responding under fixed-interval schedules of reinforcement: II. The scalloped pattern of the cumulative record. J Exp Anal Behav 29:67–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drew MR, Zupan B, Cooke A, Couvillon PA, Balsam PD (2005) Temporal control of conditioned responding in goldfish. J Exp Psychol Anim Behav Proc 31:31–39

    Article  Google Scholar 

  • Droit-Volet S (2013) Time perception in children: a neurodevelopmental approach. Neuropsychologia 51:220–234

    Article  PubMed  Google Scholar 

  • Ehrenstein WH, Ehrenstein A (1999) Modern techniques in neuroscience research. In: Windhorst U, Johansson H (eds) Psychophysical methods. Springer Verlag, Berlin, pp 1211–1241

    Google Scholar 

  • Etienne AS, Jeffrey KJ (2004) Path integration in mammals. Hippocampus 14:180–192

    Article  PubMed  Google Scholar 

  • Fetterman JG, Killeen PR (1991) Adjusting the pacemaker. Learn Motiv 22:226–252

    Article  Google Scholar 

  • Fetterman JG, Killeen PR (1992) Time discrimination in Columbia livia and Homo sapiens. J Exp Psychol 18:80–94

    CAS  Google Scholar 

  • Gallistel CR (1990) The organization of learning. MIT Press, Cambridge

    Google Scholar 

  • Gallistel CR, King A, McDonald R (2004) Sources of variability and systematic error in mouse timing behavior. J Exp Psychol Anim Behav Proc 30:3–16

    Article  CAS  Google Scholar 

  • Gellermann LW (1933) Chance orders of alternating stimuli in visual discrimination experiments. J Genet Psychol 42:206–208

    Google Scholar 

  • Gescheider GA (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, New York

    Google Scholar 

  • Gibbon J (1977) Scalar expectancy theory and Weber’s law in animal timing. Psychol Rev 84:279–325

    Article  Google Scholar 

  • Gibbon J (1991) Origins of scalar timing. Learn Motiv 22:3–38

    Article  Google Scholar 

  • Gibbon J, Church RM, Meck WH (1984) Scalar timing in memory. Ann NY Acad Sci 423:52–77

    Article  CAS  PubMed  Google Scholar 

  • Gibbon J, Malapani C, Dale CL, Gallistel CR (1997) Toward a neurobiology of temporal cognition: advances and challenges. Curr Opin Neurobiol 7:170–184

    Article  CAS  PubMed  Google Scholar 

  • 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:e103555

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 146:322–335

    Article  CAS  PubMed  Google Scholar 

  • Grondin S (2001) From physical time to the first and second moments of psychological time. Psychol Bull 127(1):22–44

    Article  CAS  PubMed  Google Scholar 

  • Grondin S (2010) Timing and time perception: a review of recent behavioral and neuroscience findings and theoretical directions. Atten Percept Psychophys 72:561–582

    Article  PubMed  Google Scholar 

  • 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 38:880–890

    Article  Google Scholar 

  • 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 17–32

    Google Scholar 

  • Grondin S, Killeen PR (2009) Tracking time with song and count: different Weber functions for musicians and nonmusicians. Atten Percept Psychophys 71:1649–1654

    Article  PubMed  Google Scholar 

  • 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 199:509–519

    Article  Google Scholar 

  • 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 92:309–318

    Article  CAS  Google Scholar 

  • Higa JJ, Simm LA (2004) Interval timing in Siamese fighting fish (Betta splendens). Behav Process 67:501–509

    Article  CAS  Google Scholar 

  • Huang J-S, Shimomura Y, Katsuura T (2012) Effects of monochromatic light on different time perception. J Hum Environ Syst 15:21–29

    Article  Google Scholar 

  • Katsuura T, Yasuda T, Shimomura Y, Iwanaga K (2007) Effects of monochromatic light on time sense for short intervals. J Physiol Anthropol 26:95–100

    Article  PubMed  Google Scholar 

  • Kleiner M, Brainard DH, Pelli DG (2007) What’s new in Psychtoolbox-3? Perception 36 (ECVP Abstract Supplement)

  • Krebs JR, Davies NB (1981) An introduction to behavioral ecology. Blackwell Scientifiy Publishing, Oxford

    Google Scholar 

  • Kuriyama K et al (2003) Circadian fluctuation of time perception in healthy human subjects. Neurosci Res 46:23–31

    Article  PubMed  Google Scholar 

  • Kuriyama K et al (2005) Diurnal fluctuation of time perception under 30-h sustained wakefulness. Neurosci Res 53:123–128

    Article  PubMed  Google Scholar 

  • Lejeune H, Wearden JH (1991) The comparative psychology of fixed-interval responding: some quantitative analyses. Learn Motiv 22:84–111

    Article  Google Scholar 

  • Lejeune H, Wearden JH (2006) Scalar properties in animal timing: conformity and violations. Q J Exp Psychol 59:1875–1908

    Article  Google Scholar 

  • 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 77:74–87

    Article  Google Scholar 

  • Maaß E (2015) Orientation in harbor seals (Phoca vitulina) – can harbor seals reproduce distances?. University of Rostock, Germany

    Google Scholar 

  • Matell MS, Meck WH (2000) Neuropsychological mechanisms of interval timing behavior. BioEssays 22:94–103

    Article  CAS  PubMed  Google Scholar 

  • 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 1–13

    Google Scholar 

  • 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 290–298

    Google Scholar 

  • Mori Y (1998) The optimal patch use in divers: optimal time budget and the number of dive cycles druing bout. J Theor Biol 190:187–199

    Article  Google Scholar 

  • 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 91:42–45

    Article  CAS  PubMed  Google Scholar 

  • Ohyama T, Gibbon J, Deich JD, Balsam PD (1999) Temporal control during maintenance and extinction of conditioned keypecking in ring doves. Anim Learn Behav 27:89–98

    Article  Google Scholar 

  • Papi F (ed) (1992) Animal homing. Animal Behaviour Series, Chapman and Hall

    Google Scholar 

  • Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437–442

    Article  CAS  PubMed  Google Scholar 

  • 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 19:1103–1109

    Article  PubMed  Google Scholar 

  • 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 24:15–33

    Article  Google Scholar 

  • Ramasco V, Biuw M, Nilssen KT (2014) Improving time budget estimates through the behavioural interpretation of dive bouts in harbour seals. Anim Behav 94:117–134

    Article  Google Scholar 

  • Richelle M, Lejeune H (1984) Timing competence and timing performance: a cross-species approach. Ann NY Acad Sci 523:254–268

    Article  Google Scholar 

  • 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 75:2063–2068

    Article  Google Scholar 

  • Rosenkilde CE, Divac I (1976) Discrimination of time intervals in cats. Acta Neurobiologica 36:311–317

    CAS  Google Scholar 

  • 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 10:257

    Article  PubMed  PubMed Central  Google Scholar 

  • Scholtyssek C, Kelber A, Dehnhardt G (2008) Brightness discrimination in the harbor seal (Phoca vitulina). Vis Res 48:96–103

    Article  PubMed  Google Scholar 

  • Scholtyssek C, Kelber A, Hanke FD, Dehnhardt G (2013) Same different concept formation in a harbor seal (Phoca vitulina). Anim Cogn 16:915–925

    Article  PubMed  Google Scholar 

  • Scholtyssek C, Kelber A, Dehnhardt G (2015) Why do seals have cones? Behavioral evidence for colorblindness in harbor seals. Anim Cogn 18:551–560

    Article  PubMed  Google Scholar 

  • 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 74:207–218

    Article  Google Scholar 

  • Stubbs A (1968) The discrimination of stimulus durations by pigeons. J Exp Anal Behav 11:225–238

    Article  Google Scholar 

  • 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 61:287–296

    Article  Google Scholar 

  • 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 27:492–501

    Article  Google Scholar 

  • Treisman M (1963) Temporal discrimination and the indifference interval: implications for a model of the “internal clock”. Psychol Monogr Gen A 77:1–31

    Article  CAS  Google Scholar 

  • Wearden JH (1991) Do humans possess an internal clock with scalar timing properties? Learn Mem 22:59–83

    Google Scholar 

  • 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 214:1922–1930

    Article  PubMed  Google Scholar 

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Acknowledgments

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.

Funding

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

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Authors and Affiliations

  1. Institute for Biosciences, Sensory and Cognitive Ecology, University of Rostock, Albert-Einstein-Str. 3, 18059, Rostock, Germany

    Tamara Heinrich, Guido Dehnhardt & Frederike D. Hanke

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  1. Tamara Heinrich
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  2. Guido Dehnhardt
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  3. Frederike D. Hanke
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Correspondence to Frederike D. Hanke.

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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.

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Heinrich, T., Dehnhardt, G. & Hanke, F.D. Harbour seals (Phoca vitulina) are able to time precisely. Anim Cogn 19, 1133–1142 (2016). https://doi.org/10.1007/s10071-016-1020-3

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