Skip to main content

Advertisement

Log in

Variability in the “stereotyped” prey capture sequence of male cuttlefish (Sepia officinalis) could relate to personality differences

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Studies of animal personality have shown consistent between-individual variation in behaviour in many social and non-social contexts, but hunting behaviour has been overlooked. Prey capture sequences, especially in invertebrates, are supposed to be quite invariant. In cuttlefish, the attack includes three components: attention, positioning, and seizure. The previous studies indicated some variability in these components and we quantified it under the hypothesis that it could relate to personality differences. We, therefore, analysed predation sequences of adult cuttlefish to test their association with personality traits in different contexts. Nineteen subjects were first exposed to an “alert” and a “threat” test and then given a live prey, for 10 days. Predation sequences were scored for components of the attack, locomotor and postural elements, body patterns, and number of successful tentacle ejections (i.e. seizure). PCA analysis of predatory patterns identified three dimensions accounting for 53.1%, 15.9%, and 9.6% of the variance and discriminating individuals based on “speed in catching prey”, “duration of attack behaviour”, and “attention to prey”. Predation rate, success rate, and hunting time were significantly correlated with the first, second, and third PCA factors, respectively. Significant correlations between capture patterns and responsiveness in the alert and threat tests were found, highlighting a consistency of prey capture patterns with measures of personality in other contexts. Personality may permeate even those behaviour patterns that appear relatively invariant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Adamo SA, Ehgoetz K, Sangster C, Whitehorne I (2006) Signaling to the enemy? Body pattern expression and its response to external cue during hunting in the cuttlefish Sepia officinalis (Cephalopoda). Biol Bull 210:192–200

    Article  Google Scholar 

  • Anderson RC, Mather JA, Steele CW (2004) Burying and associated behaviors of Rossia pacifica (Cephalopoda: Sepiolidae). Vie et Milieu Serie A Biologie Marine 54:13–19

    Google Scholar 

  • Araujo MS, Bolnick DI, Martinelli LA, Giaretta AA, dos Reis SF (2009) Individual-level diet variation in four species of Brazilian frogs. J Anim Ecol 78:848–856

    Article  CAS  Google Scholar 

  • Barlow GW (1968) Ethological units of behaviour. In: Ingle D (ed) The central nervous system and fish behaviour. University of Chicago Press, Chicago, pp 217–237

    Google Scholar 

  • Barlow GW (1977) Modal action patterns. In: Sebeok TA (ed) How animals communicate. Indiana University Press, Bloomington, pp 98–134

    Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  Google Scholar 

  • Berridge KC (1990) Comparative fine-structure of action-rules of form and sequence in the grooming patterns of 6 rodent species. Behaviour 113:21–56

    Article  Google Scholar 

  • Boal JG, Wittenberg KM, Hanlon RT (2000) Observational learning does not explain improvement in predation tactics by cuttlefish (Mollusca: Cephalopoda). Behav Proc 52:141–153

    Article  Google Scholar 

  • Bonner JT (1980) The evolution of culture in animals. Princeton University Press, Princeton

    Google Scholar 

  • Boycott BB (1953) The chromatophore system of cephalopods. Proc Linn Soc Lond 164:235–240

    Article  Google Scholar 

  • Boycott BB (1958) The cuttlefish—Sepia. New Biol 25:98–118

    Google Scholar 

  • Brown C, Garwood MP, Williamson JE (2012) It pays to cheat: tactical deception in a cephalopod social signaling system. Biol Lett 8:729–732

    Article  Google Scholar 

  • Carere C, Eens M (2005) Unravelling animal personalities: how and why individuals consistently differ. Behaviour 142:1149–1157

    Article  Google Scholar 

  • Carere C, Maestripieri D (eds) (2013) Animal personalities: behavior physiology and evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Carere C, Grignani G, Bonanni R, Della Gala M, Carlini A, Angeletti D, Cimmaruta R, Nascetti G, Mather JA (2015) Consistent individual differences in the behavioural responsiveness of adult male cuttlefish (Sepia officinalis). Appl Anim Behav Sci 167:89–95

    Article  Google Scholar 

  • Chittka L, Skorupski P, Raine NE (2009) Speed-accuracy tradeoffs in animal decision making. Trends Ecol Evol 24(7):400–407

    Article  Google Scholar 

  • Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936

    Article  CAS  Google Scholar 

  • Costantini D, Casagrande S, Di Lieto G, Fanfani A, Dell’Omo G (2005) Consistent differences in feeding habits between neighbouring breeding kestrels. Behaviour 142:1403–1415

    Article  Google Scholar 

  • Crossland MR (2001) Ability of predatory native Australian fishes to learn to avoid toxic larvae of the introduced toad Bufo marinus. J Fish Biol 59:319–329

    Article  Google Scholar 

  • Darmaillacq AS, Dickel L, Chichery MP, Chichery R (2004) Rapid taste aversion learning in adult cuttlefish Sepia officinalis. Anim Behav 68:1291–1298

    Article  Google Scholar 

  • Darmaillacq AS, Jozet-Alves C, Bellanger C, Dickel L (2014) Cuttlefish preschool or how to learn in the peri-hatching period. In: Darmaillacq AS, Dickel L, Mather JM (eds) Cephalopod cognition. Cambridge University Press, Cambridge, pp 3–30

    Chapter  Google Scholar 

  • Dickel L, Chichery MP, Chichery R (1997) Postembryonic maturation of the vertical lobe complex and early development of predatory behavior in the cuttlefish (Sepia officinalis). Neurobiol Learn Mem 67:150–160

    Article  CAS  Google Scholar 

  • Dixon LM, Duncan IJH, Mason G (2008) What’s in a peck? Using fixed action pattern morphology to identify the motivational basis of abnormal feather-pecking behaviour. Anim Behav 76:1035–1042

    Article  Google Scholar 

  • Duval P, Chichery MP, Chichery R (1984) Prey capture by the cuttlefish (Sepia officinalis L): an experimental study of two strategies. Behav Proc 9:13–21

    Article  CAS  Google Scholar 

  • Ferrari C, Pasquaretta C, Carere C, Cavallone E, von Hardenberg A, Reale D (2013) Testing for the presence of coping styles in a wild mammal. Anim Behav 85:1385–1396

    Article  Google Scholar 

  • Fiorito G, Affuso A, Anderson DB, Basil J, Bonnaud L, Botta G, Cole A et al (2014) Cephalopods in neuroscience: regulations research and the 3Rs. Invertebr Neurosci 14:13–36

    Article  CAS  Google Scholar 

  • Fiorito G, Affuso A, Basil J, Cole A, de Girolamo P, D’Angelo L, Dickel L et al (2015) Guidelines for the care and welfare of cephalopods in research—a consensus based on an initiative by CephRes FELASA and the Boyd Group. Lab Anim 49:1–90

    Article  Google Scholar 

  • Flash T, Hochner B (2005) Motor primitives in vertebrates and invertebrates. Curr Opin Neurobiol 15:660–666

    Article  CAS  Google Scholar 

  • Giuliani A (2017) The application of principal component analysis to drug discovery and biomedical data. Drug Discov Today 22:1069–1076

    Article  CAS  Google Scholar 

  • Giuliani A, Ghirardi O, Caprioli A, Di Serio S, Ramacci MT, Angelucci L (1994) Multivariate analysis of behavioural aging highlights some unexpected features of complex systems organization. Behav Neural Biol 61:110–122

    Article  CAS  Google Scholar 

  • Giuliani A, Zbilut JP, Conti F, Manetti C, Miccheli A (2004) Invariant features of metabolic networks: a data analysis application on scaling properties of biochemical pathways. Phys A 337:157–170

    Article  CAS  Google Scholar 

  • Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86

    Article  CAS  Google Scholar 

  • Griffin A, Healy SD, Guillette LM (2015) Cognition and personality: an analysis of an emerging field. Trends in Ecology Evolution 30:207–214

    Article  Google Scholar 

  • Groothuis TGG, Carere C (2005) Avian personalities: characterisation and epigenesist. Neurosci Biobehav Re 29:137–150

    Article  Google Scholar 

  • Guerra A (2006) Ecology of Sepia officinalis. Vie et Milieu Serie A Biologie Marine 56:97–107

    Google Scholar 

  • Guillette LM, Naguib M, Griffin AS (2017) Individual differences in behaviour and cognition. Behav Proc 134:1–3

    Article  Google Scholar 

  • Hanlon RT, Messenger JB (1988) Adaptive coloration in young cuttlefish (Sepia officinalis L.): the morphology and development of body patterns and their relation to behaviour. Philos Trans R Soc Lond Ser B 320:437–487

    Article  Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Holmes W (1940) The colour and the colour patterns of Sepia officinalis. Proc Zool Soc Lond 110:17–36

    Google Scholar 

  • Horvath K, Angeletti D, Nascetti G, Carere C (2013) Invertebrate welfare: an overlooked issue. Annali dell’Istituto Superiore di Sanità 49:9–17

    PubMed  Google Scholar 

  • Huntingford FA (1984) Some ethical issues raised by studies of predation and aggression. Anim Behav 32:210–215

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • Lorenz K, Tinbergen N (1938) Taxis and instinctive behaviour pattern in egg-rolling by the Greylag goose. In: Lorenz K (ed) Studies in animal and human behaviour, vol 1. Harvard University Press, Cambridge, pp 316–350

    Google Scholar 

  • Mather JA (1986) Sand-digging in Sepia officinalis: assessment of a cephalopod mollusc’s “fixed” behavior pattern. J Comp Psychol 100:315–320

    Article  Google Scholar 

  • Mather JA (2011) Consciousness in cephalopods? J Cosmol 14:4472–4483

    Google Scholar 

  • Mather JA, Anderson RC (1993) Personalities of Octopuses (Octopus rubescens). J Comp Psychol 107:336–340

    Article  Google Scholar 

  • Mather JA, Carere C (2018) Consider the individual: personality and welfare in invertebrate animals. In: Carere C, Mather JA (eds) The welfare of invertebrate animals. Springer International Publishing, Cham (in press)

    Google Scholar 

  • Mather JA, Logue DM (2013) The bold and the spineless: approaches to personality in invertebrates. In: Carere C, Maestripieri D (eds) Animal personalities: behavior physiology and evolution. University of Chicago Press, Chicago (IL), pp 13–35

    Google Scholar 

  • Mather JA, Leite TS, Batista AT (2012) Individual prey choices of octopuses: are they generalist or specialist? Curr Zool 58:597–603

    Article  Google Scholar 

  • Messenger JB (1968) The visual attack of the cuttlefish Sepia officinalis. Anim Behav 16:342–357

    Article  CAS  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045

    Article  Google Scholar 

  • Natoli E, Say L, Cafazzo S, Bonanni R, Schmid M, Pointier D (2005) Bold attitude makes urban feral domestic cats more vulnerable to feline immunodeficiency virus. Neurosci Biobehav Rev 29:151–157

    Article  Google Scholar 

  • O’Brien CE, Mezrai N, Darmaillacq AS, Dickel L (2016) Behavioral development in embryonic and early juvenile cuttlefish (Sepia officinalis). Dev Psychobiol 9999:1–16

    Google Scholar 

  • Pronk R, Wilson DR, Harcourt R (2010) Video playback demonstrates episodic personality in the gloomy octopus. J Exp Biol 213:1035–1041

    Article  CAS  Google Scholar 

  • Reale D, Reader SM, Sol D, McDougall OT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  Google Scholar 

  • Sanders FK, Young JZ (1940) Learning and other functions of the higher nervous centres of Sepia. J Neurophysiol 3:501–526

    Article  Google Scholar 

  • Sih A, Del Giudice M (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc B 367:2762–2772

    Article  Google Scholar 

  • Sih A, Bell A, Chadwick JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  Google Scholar 

  • Sinn DL, Moltschaniwskyji NA (2005) Personality traits in dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. J Comp Psychol 119:99–110

    Article  Google Scholar 

  • Sinn D, Perrin N, Mather JA, Anderson RC (2001) Early temperamental traits in an octopus (Octopus bimaculoides). J Comp Psychol 115:351–364

    Article  CAS  Google Scholar 

  • Smith JA, Andrews PLR, Hawkins P, Louhimies S, Ponte G, Dickel L (2013) Cephalopod research and EU Directive 2010/63/EU: requirements impacts and ethical review processes. J Exp Mar Biol Ecol 447:31–45

    Article  Google Scholar 

  • Tetley CL, O’Hara SJ (2012) Rating of personality as a tool for improving the breeding management and welfare of zoo animals. Anim Welf 21:463–476

    Article  CAS  Google Scholar 

  • Tonkins BM, Tyers AM, Cooke GM (2015) Cuttlefish in captivity: an investigation into housing and husbandry for improving welfare. Appl Anim Behav Sci 168:77–83

    Article  Google Scholar 

  • van Hierden YM, Korte SM, Ruesink EW, van Reenen CG, Engel B, Koolhaas JM, Blokhuis HJ (2002) The development of feather pecking behaviour and targeting of pecking in chicks from a high and low feather pecking line of laying hens. Appl Anim Behav Sci 77:183–196

    Article  Google Scholar 

  • van Oers K, de Jong G, Drent PJ, van Noordwijk AJ (2004) Genetic correlations of avian personality traits: correlated response to artificial selection. Behav Genet 34:611–619

    Article  Google Scholar 

  • von Boletzky S, Hanlon RT (1983) A review of the laboratory maintenance rearing and culture of cephalopod molluscs. Mem Natl Mus Vic 44:147–187

    Article  Google Scholar 

  • Wells MJ (1958) Factors affecting reactions to mysis by newly hatched Sepia. Behaviour 13:96–111

    Article  Google Scholar 

  • Wilson DP (1946) A note on the capture of prey by Sepia officinalis L. J Mar Biol Assoc UK 26:421–425

    Article  Google Scholar 

  • Yang T-I, Chiao C-C (2016) Number sense and state-dependent valuation in cuttlefish. Proc R Soc B Biol Sci 283:20161379

    Article  Google Scholar 

Download references

Acknowledgements

This research was partially supported by a Marie Skłodowska-Curie Individual Fellowships (H2020-MSCA-IF-2014), Project ID: 659106 (GROUPIND), to C. Carere. We wish to thank A. Giuliani and F. Chiarotti for statistical advice, N. Francia and S. Falsini for precious technical and administrative support. The work is part of the BSc thesis of G. Cordeschi. Finally, we wish to thank the authors of the original study (Carere et al. 2015).

Funding

This study was funded by H2020-MSCA-IF-2014 (GROUPIND), Grant number 659106.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francesca Zoratto.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All international, national, and/or institutional guidelines for the care and use of animals, applicable when the original study by Carere et al. (2015) was performed, were followed. Specifically, the original study complied with the regulations of the Canadian Council of Animal Care for animal research (University of Lethbridge, Animal Welfare Approval n. 1106).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 1045 KB)

Supplementary material 2 (DOCX 35 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zoratto, F., Cordeschi, G., Grignani, G. et al. Variability in the “stereotyped” prey capture sequence of male cuttlefish (Sepia officinalis) could relate to personality differences. Anim Cogn 21, 773–785 (2018). https://doi.org/10.1007/s10071-018-1209-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-018-1209-8

Keywords

Navigation