Skip to main content
Log in

The underestimated giants: operant conditioning, visual discrimination and long-term memory in giant tortoises

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

Abstract

Relatively little is known about cognition in turtles, and most studies have focused on aquatic animals. Almost nothing is known about the giant land tortoises. These are visual animals that travel large distances in the wild, interact with each other and with their environment, and live extremely long lives. Here, we show that Galapagos and Seychelle tortoises, housed in a zoo environment, readily underwent operant conditioning and we provide evidence that they learned faster when trained in the presence of a group rather than individually. The animals readily learned to distinguish colors in a two-choice discrimination task. However, since each animal was assigned its own individual colour for this task, the presence of the group had no obvious effect on the speed of learning. When tested 95 days after the initial training, all animals remembered the operant task. When tested in the discrimination task, most animals relearned the task up to three times faster than naïve animals. Remarkably, animals that were tested 9 years after the initial training still retained the operant conditioning. As animals remembered the operant task, but needed to relearn the discrimination task constitutes the first evidence for a differentiation between implicit and explicit memory in tortoises. Our study is a first step towards a wider appreciation of the cognitive abilities of these unique animals.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bitterman ME (1965) Phyletic differences in learning. Am Psychol 20:396–410

    Article  CAS  Google Scholar 

  • Bitterman ME (1975) The comparative analysis of Learning. Science 188:699–709

    Article  CAS  Google Scholar 

  • Brown C, Laland K, Krause J (2011) Fish cognition and behaviour. Wiley-Blackwell, Oxford. https://doi.org/10.1002/9781444342536

    Book  Google Scholar 

  • Burghardt GM (1977) Learning processes in reptiles. In: Gans C, Tinkle D (eds) The biology of the reptilia. Ecology the behavior part A, vol 7. Academic Press, New York

    Google Scholar 

  • Darwin C (1878) Journal of researches into the natural history and geology of the countries visited during the voyage of H.M.S Beagle round the world. 2nd edn. D. Appleton and company, New York, pp 382–385

  • Davis KM, Burghardt GM (2007) Training and long-term memory of a novel food acquisition task in a turtle (Pseudemys nelsoni). Behav Process 75:225–230

    Article  Google Scholar 

  • Davis KM, Burghardt GM (2011) Turtles (Pseudemys nelsoni) learn about visual cues indicating food from experienced turtles. J Comp Psychol 125:404–410

    Article  Google Scholar 

  • Delano A (1817) Narrative of voyages and travels in the northern and southern hemispheres: comprising three voyages round the world; together with a voyage of survey and discovery, in the Pacific Ocean and oriental islands. 1st edn. E. G. House

  • Denbrurgh JV (1914) The gigantic land tortoises of the Galapagos archipelago. Proc Calif Acad Sci 2:203–374

    Google Scholar 

  • Desmond T, Laule G (1998) Positive reinforcement as an enrichment strategy. In: Shepherdson DJ, Mellen JD, Hutchins M (eds) Second nature: environmental enrichment for captive animals. Smithsonian Institution Press, Washington, pp 302–314

    Google Scholar 

  • El’darov AL, Sikharulidze NI (1968) Concerning studies of marsh tortoise behaviour. Proc Acad Sci USSR 182:237–239

    Google Scholar 

  • Evans LT, Quaranta JV (1949) Patterns of cooperative behavior in a herd of 14 giant tortoises at the Bronx Zoo. Anat Rec 105:506

    Google Scholar 

  • Fernandes EJ, Timberlake W (2008) Mutual benefits of research collaborations between zoos and academic institutions. Zoo Biol 27:470–487

    Article  Google Scholar 

  • Fellows BJ (1967) Change stimulus sequences for discrimination tasks. Psychol Bull 67:87–92

    Article  CAS  Google Scholar 

  • Fiorito G, Scotto P (1992) Observational learning in Octopus vulgaris. Science 256:545–547

    Article  CAS  Google Scholar 

  • Gaalema DE, Benboe D (2008) Positive reinforcement training of Aldabra tortoises (Geochelone gigantea) at Zoo Atlanta. Herp Rev 39:331–334

    Google Scholar 

  • Grandin T, Rooney MB, Phillips M, Cambre RC, Irlbeck NA, Graffem W (1995) Conditioning of Nyala (Tragelaphus angasi) to blood sampling in a crate with positive reinforcement. Zoo Biol 14:261–273

    Article  Google Scholar 

  • Grubb P (1971) The growth, ecology and population structure of giant tortoises on Aldabra. Philos Trans R Soc Lond B 260:327–372

    Article  Google Scholar 

  • Harless M, Morlock H (1979) Turtles: perspectives and research. Wiley, New York

    Google Scholar 

  • Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231

    Article  CAS  Google Scholar 

  • Hoppitt W, Laland N (2008) Social processes influencing learning in animals: a review of the evidence. Adv Study Behav 38:105–165

    Article  Google Scholar 

  • Huber L, Range F, Voelkl B, Szucsich ZV, Miklosi A (2009) The evolution of imitation: what do the capacities of non-human animals tell us about the mechanisms of imitation? Philos Trans R Soc Lond B Biol Sci 364:2299–2309

    Article  Google Scholar 

  • Kis A, Huber L, Wilkinson A (2015) Social learning by imitation in a reptile (Pogona vitticeps). Anim Cogn 18:325–331

    Article  Google Scholar 

  • Laland KN, Brown C, Krause J (2003) Learning in fishes: from three-seconds memory to culture. Fish Fish 4:192–202

    Article  Google Scholar 

  • Leadbeater E, Chittka L (2007) Social learning in insects—from miniature brains to consensus building. Curr Biol 17:703–713

    Article  Google Scholar 

  • Matsubara S, Deeming DC, Wilkinson A (2017) Cold-blooded cognition: new directions in reptile cognition. Curr Opin Behav Sci 16:126–130

    Article  Google Scholar 

  • Phillips M, Grandin T, Graftam W, Iribeck NA, Cambre RC (1998) Crate conditioning of bongo (Tragelaphus eurycerus) for Veterinary and husbandry procedures at the Denver zoological gardens. Zoo Biol 17:25–32

    Article  Google Scholar 

  • Schacter DL (1987) Implicit memory: history and current status. J Exp Psychol 13:501–518

    Google Scholar 

  • Schatz P (2011) Forced-choice test. In: Kreutzer JS, DeLuca J, Caplan B (eds) Encyclopedia of clinical neuropsychology. Springer, New York. https://doi.org/10.1007/978-0-387-79948-3

    Chapter  Google Scholar 

  • Slagsvold T, Wiebe KL (2011) Social learning in birds and its role in shaping a foraging niche. Philos Trans R Soc Lond B Biol Sci 366:969–977

    Article  Google Scholar 

  • Soldati F, Burman OHP, John EA, Pike TW, Wilkinson A (2017) Long-term memory of relative reward values. Biol Lett 13:20160853

    Article  Google Scholar 

  • Thonhauser KE, Gutnick T, Byrne RA, Kral K, Burghardt GM, Kuba MJ (2013) Social learning in Cartilaginous fish (stingrays Potamotrygon falkneri). Anim Cogn 16:927–932

    Article  Google Scholar 

  • Thorndike EL (1911) Animal intelligence. Macmillan, New York

    Google Scholar 

  • Thorpe WH (1963) Learning and instinct in animals, 2nd edn. Methuen, London

    Google Scholar 

  • Weiss E, Wilson S (2003) The use of classical and operant conditioning in training Aldabra tortoises (Geochelone gigantea) for venipuncture and other husbandry issues. J Appl Anim Welf Sci 6:33–38

    Article  CAS  Google Scholar 

  • Wilkinson A, Huber L (2012) Cold-blooded cognition: reptilian cognitive abilities. In: Vonk J, Shackelfor TK (eds) The Oxford handbook of comparative evolutionary psychology. Oxford University Press, Oxford Township, pp 129–143

    Google Scholar 

  • Wilkinson A, Kuenstner K, Mueller J, Huber L (2010a) Social Learning in a non- social reptile (Geochelone carbonaria). Biol Lett 6:614–616

    Article  Google Scholar 

  • Wilkinson A, Mandl I, Bugnyar T, Huber L (2010b) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769

    Article  Google Scholar 

  • Yerkes RM (1901) The formation of habits in the turtle. Popul Sci Mon 58:519–525

    Google Scholar 

Download references

Acknowledgements

We want to thank the Vienna Zoo animal keeper team in the Aquarium house who supported and enriched this project with their help and ideas and the Elephant house and keepers for housing the tortoises and us for part of the experiment. The curators and the keepers at the Zürich zoo were essential for the completion of the work at their institution.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Tamar Gutnick or Michael J. Kuba.

Ethics declarations

Conflict of interest

T Gutnick has received an honorarium from Tiergarten Schönbrunn supported by donation from H.H. Lederer.

Ethical approval

All applicable international, national and institutional guidelines for care and use of animals were followed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Video SV1: Male Aldabra Tortoise training for Stage 2 - go to ball (MOV 18376 kb)

Supplementary Video SV2: Stage 3 - Color discrimination: Female Galapagos tortoise performing correct trial. Note the visual barrier in the background (MOV 21878 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gutnick, T., Weissenbacher, A. & Kuba, M.J. The underestimated giants: operant conditioning, visual discrimination and long-term memory in giant tortoises. Anim Cogn 23, 159–167 (2020). https://doi.org/10.1007/s10071-019-01326-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-019-01326-6

Keywords

Navigation