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.
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Bitterman ME (1965) Phyletic differences in learning. Am Psychol 20:396–410
Bitterman ME (1975) The comparative analysis of Learning. Science 188:699–709
Brown C, Laland K, Krause J (2011) Fish cognition and behaviour. Wiley-Blackwell, Oxford. https://doi.org/10.1002/9781444342536
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
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
Davis KM, Burghardt GM (2011) Turtles (Pseudemys nelsoni) learn about visual cues indicating food from experienced turtles. J Comp Psychol 125:404–410
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
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
El’darov AL, Sikharulidze NI (1968) Concerning studies of marsh tortoise behaviour. Proc Acad Sci USSR 182:237–239
Evans LT, Quaranta JV (1949) Patterns of cooperative behavior in a herd of 14 giant tortoises at the Bronx Zoo. Anat Rec 105:506
Fernandes EJ, Timberlake W (2008) Mutual benefits of research collaborations between zoos and academic institutions. Zoo Biol 27:470–487
Fellows BJ (1967) Change stimulus sequences for discrimination tasks. Psychol Bull 67:87–92
Fiorito G, Scotto P (1992) Observational learning in Octopus vulgaris. Science 256:545–547
Gaalema DE, Benboe D (2008) Positive reinforcement training of Aldabra tortoises (Geochelone gigantea) at Zoo Atlanta. Herp Rev 39:331–334
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
Grubb P (1971) The growth, ecology and population structure of giant tortoises on Aldabra. Philos Trans R Soc Lond B 260:327–372
Harless M, Morlock H (1979) Turtles: perspectives and research. Wiley, New York
Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231
Hoppitt W, Laland N (2008) Social processes influencing learning in animals: a review of the evidence. Adv Study Behav 38:105–165
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
Kis A, Huber L, Wilkinson A (2015) Social learning by imitation in a reptile (Pogona vitticeps). Anim Cogn 18:325–331
Laland KN, Brown C, Krause J (2003) Learning in fishes: from three-seconds memory to culture. Fish Fish 4:192–202
Leadbeater E, Chittka L (2007) Social learning in insects—from miniature brains to consensus building. Curr Biol 17:703–713
Matsubara S, Deeming DC, Wilkinson A (2017) Cold-blooded cognition: new directions in reptile cognition. Curr Opin Behav Sci 16:126–130
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
Schacter DL (1987) Implicit memory: history and current status. J Exp Psychol 13:501–518
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
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
Soldati F, Burman OHP, John EA, Pike TW, Wilkinson A (2017) Long-term memory of relative reward values. Biol Lett 13:20160853
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
Thorndike EL (1911) Animal intelligence. Macmillan, New York
Thorpe WH (1963) Learning and instinct in animals, 2nd edn. Methuen, London
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
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
Wilkinson A, Kuenstner K, Mueller J, Huber L (2010a) Social Learning in a non- social reptile (Geochelone carbonaria). Biol Lett 6:614–616
Wilkinson A, Mandl I, Bugnyar T, Huber L (2010b) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769
Yerkes RM (1901) The formation of habits in the turtle. Popul Sci Mon 58:519–525
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.
Conflict of interest
T Gutnick has received an honorarium from Tiergarten Schönbrunn supported by donation from H.H. Lederer.
All applicable international, national and institutional guidelines for care and use of animals were followed.
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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
- Operant learning
- Visual discrimination learning
- Long-term memory
- Aldabra tortoise
- Galapagos tortoise