Abstract
To gain a better understanding of the evolution of animal cognition, it is necessary to test and compare the cognitive abilities of a broad array of taxa. Meaningful inter-species comparisons are best achieved by employing universal paradigms that standardize testing among species. Many cognitive paradigms, however, have been tested in only a few taxa, mostly birds and primates. One such example, known as the Aesop’s Fable paradigm, is designed to assess causal understanding in animals using water displacement. To evaluate the universal effectiveness of the Aesop’s Fable paradigm, we applied this paradigm to a previously untested taxon, the raccoon (Procyon lotor). We first trained captive raccoons to drop stones into a tube of water to retrieve a floating food reward. Next, we presented successful raccoons with objects that differed in the amount of water they displaced to determine whether raccoons could select the most functional option. Raccoons performed differently than corvids and human children did in previous studies of Aesop’s Fable, and we found raccoons to be innovative in many aspects of this task. We suggest that raccoon performance in this paradigm reflected differences in tangential factors, such as behavior, morphology, and testing procedures, rather than cognitive deficiencies. We also present insight into previously undocumented challenges that should better inform future Aesop’s Fable studies incorporating more diverse taxa.
References
Auersperg AMI, Gajdon GK, von Bayern AMP (2012) A new approach to comparing problem solving, flexibility and innovation. Commun Integr Biol 5:140–145. doi:10.4161/cib.18787
Benson-Amram S, Holekamp KE (2012) Innovative problem solving by wild spotted hyenas. Proc R Soc B Biol Sci 279:4087–4095. doi:10.1098/rspb.2012.1450
Benson-Amram S, Dantzer B, Stricker G et al (2016) Brain size predicts problem-solving abilities in mammalian carnivores. Proc Natl Acad Sci. doi:10.1073/pnas.1505913113
Bird CD, Emery NJ (2009) Rooks use stones to raise the water level to reach a floating worm. Curr Biol 19:1410–1414. doi:10.1016/j.cub.2009.07.033
Breland K, Breland M (1961) The misbehavior of organisms. Am Psychol 16:681–684. doi:10.1037/h0040090
Cheke LG, Bird CD, Clayton NS (2011) Tool-use and instrumental learning in the Eurasian jay (Garrulus glandarius). Anim Cognit 14:441–455. doi:10.1007/s10071-011-0379-4
Cheke LG, Loissel E, Clayton NS (2012) How do children solve Aesop’s fable? PLoS ONE. doi:10.1371/journal.pone.0040574
Chow PKY, Lea SEG, Leaver LA (2016) How practice makes perfect: the role of persistence, flexibility and learning in problem-solving efficiency. Anim Behav 112:273–283. doi:10.1016/j.anbehav.2015.11.014
Cole LW (1907) Concerning the intelligence of raccoons. J Comp Neurol Psychol 17:211–261
Daniels S (2016) Behavioral flexibility of a generalist carnivore. Master’s Thesis, University of Wyoming
Davis HB (1907) The raccoon: a study in animal intelligence. Am J Psychol 18:447–489
Jacobs IF, Osvath M (2015) The string-pulling paradigm in comparative psychology. J Comp Psychol 129:89–120. doi:10.1037/a0038746
Jelbert SA, Taylor AH, Cheke LG et al (2014) Using the Aesop’s Fable paradigm to investigate causal understanding of water displacement by New Caledonian crows. PLoS ONE 9:e92895. doi:10.1371/journal.pone.0092895
Jelbert SA, Taylor AH, Gray RD (2015) Investigating animal cognition with the Aesop’s Fable paradigm: current understanding and future directions. Commun Integr Biol 8:1–6. doi:10.1080/19420889.2015.1035846
Johnson SR, Crider NJ, Weyer GA et al (2016) Bait development for oral delivery of pharmaceuticals to raccoons (Procyon lotor) and striped skunks (Mephitis mephitis). J Wildl Dis 52:893–901. doi:10.7589/2015-12-322
Logan CJ (2016) Behavioral flexibility and problem solving in an invasive bird. PeerJ 4:e1975. doi:10.7717/peerj.1975
Logan CJ, Jelbert SA, Breen AJ et al (2014) Modifications to the Aesop’s Fable paradigm change New Caledonian crow performances. PLoS ONE 9:1–9. doi:10.1371/journal.pone.0103049
Logan CJ, Harvey BD, Schlinger BA, Rensel M (2016) Western scrub-jays do not appear to attend to functionality in Aesop’s Fable experiments. PeerJ 4:e1707. doi:10.7717/peerj.1707
Mendes N, Hanus D, Call J (2007) Raising the level: orangutans use water as a tool. Biol Lett 3:453–455. doi:10.1098/rsbl.2007.0198
Miller R, Jelbert SA, Taylor AH et al (2016) Performance in object-choice Aesop’s Fable Tasks are influenced by object biases in New Caledonian crows but not in human children. PLoS ONE 11:e0168056. doi:10.1371/journal.pone.0168056
North S (1966) Raccoons are the brightest people. E.P. Dutton & Co., Inc., New York
Shettleworth SJ (2010) Cognition, evolution, and behaviour, 2nd edn. Oxford University Press, New York
Taylor AH, Elliffe DM, Hunt GR et al (2011) New Caledonian crows learn the functional properties of novel tool types. PLoS ONE. doi:10.1371/journal.pone.0026887
Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Philos Trans R Soc B Biol Sci 367:2773–2783. doi:10.1098/rstb.2012.0214
Visalberghi E, Limongelli L (1994) Lack of comprehension of cause-effect relations in tool-using capuchin monkeys (Cebus apella). J Comp Psychol 108:15–22. doi:10.1037/0735-7036.108.1.15
Vonk J, Leete J (2017) Carnivore concepts: categorization in carnivores “bears” further study. Int J Comp Psychol 30:1–20. doi:10.5811/westjem.2011.5.6700
Acknowledgements
We thank the National Wildlife Research Center’s animal care managers and staff for their assistance with this research, and Brett Jesmer for his assistance with analyses. We also thank Kyle Stickelman and the Arts and Sciences Division of Research Support at the University of Wyoming (UW) for their help with the design and construction of our Aesop’s Fable apparatus. This study was partially funded by the UW Department of Zoology and Physiology L. Floyd Clarke Graduate Scholar Award to L.S.
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Online Resource 1: Video footage from Raccoon 29’s seventh learning trial. Here we see that when he touches the apparatus, stones balanced on top of the tube fall in, raising the water level to a point where he can reach in and obtain the floating marshmallow reward (MP4 74935 kb)
Online Resource 2: Video footage from Raccoon 29’s second substrate trial. He first drops a stone into the water tube, retrieves and eats a piece of marshmallow, then selects a second stone and drops it into the corncob tube. After he is unable to obtain the reward from the corncob tube, he returns to the pile of stones, makes a selection, and heads toward the water tube (MP4 9610 kb)
Online Resource 3: Video footage from Raccoon 40’s eleventh density trial. He begins by picking up a dense ball and placing it on the rim of the apparatus. He then selects a second ball, and as he brings it to the rim he knocks the first, dense ball into the tube. The ball’s impact on the surface of the water causes a few, small pieces of marshmallow to eject out of the tube. After Raccoon 40 finishes eating the ejected marshmallow, he drops the second, dense ball into the tube and retrieves the reward (MP4 61733 kb)
Online Resource 4: Video footage from Raccoon 29’s eleventh tool use trial. He moves the cup around the opening of the tube with his paws and mouth for several seconds before releasing it into the tube. He then quickly grabs the handle of the cup before it sinks, and retrieves a piece of marshmallow as he pulls the cup out of the tube (MP4 12548 kb)
Online Resource 5: Video footage from Raccoon 22’s fourth final trial. Here we see that she is able to overturn the entire apparatus by rocking her body backwards while pulling on the rim of the tube. We designed the apparatus to be freestanding so that the raccoons could approach and explore the apparatus from all sides. Thus, we made the base of the apparatus smooth, lacking any raised edges, and heavy (11.3 kg) so that the raccoons would not be able to grip or lift the base. Despite these precautions, Raccoon 22 was able to overturn it and retrieve the reward (MP4 87361 kb)
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Stanton, L., Davis, E., Johnson, S. et al. Adaptation of the Aesop’s Fable paradigm for use with raccoons (Procyon lotor): considerations for future application in non-avian and non-primate species. Anim Cogn 20, 1147–1152 (2017). https://doi.org/10.1007/s10071-017-1129-z
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DOI: https://doi.org/10.1007/s10071-017-1129-z