Abstract
Trait heritability is necessary for evolution by both natural and artificial selection, yet we know little about the heritability of cognitive traits. Domestic dogs are a valuable study system for questions regarding the evolution of phenotypic diversity due to their extraordinary intraspecific variation. While previous studies have investigated morphological and behavioral variation across dog breeds, few studies have systematically assessed breed differences in cognition. We integrated data from Dognition.com—a citizen science project on dog cognition—with breed-averaged genetic data from published sources to estimate the among-breed heritability of cognitive traits using mixed models. The resulting dataset included 11 cognitive measures for 1508 adult dogs across 36 breeds. A factor analysis yielded four factors interpreted as reflecting inhibitory control, communication, memory, and physical reasoning. Narrow-sense among-breed heritability estimates—reflecting the proportion of cognitive variance attributable to additive genetic variation—revealed that scores on the inhibitory control and communication factors were highly heritable (inhibitory control: h2 = 0.70; communication: h2 = 0.39), while memory and physical reasoning were less heritable (memory: h2 = 0.17; physical reasoning: h2 = 0.21). Although the heritability of inhibitory control is partially explained by body weight, controlling for breed-average weight still yields a high heritability estimate (h2 = 0.50), while other factors are minimally affected. Our results indicate that cognitive phenotypes in dogs covary with breed relatedness and suggest that cognitive traits have strong potential to undergo selection. The highest heritabilities were observed for inhibitory control and communication, both of which are hypothesized to have been altered by domestication.
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References
Akdemir D, Godfrey OU (2015) EMMREML: fitting mixed models with known covariance structures. https://cran.r-project.org/package=EMMREML
American Kennel Club (1938) The complete dog book. Halcyon House, New York
Arden R, Adams MJ (2016) A general intelligence factor in dogs. Intelligence 55:79–85. https://doi.org/10.1016/j.intell.2016.01.008
Arden R, Bensky MK, Adams MJ (2016) A review of cognitive abilities in dogs, 1911 through 2016: more individual differences, please! Curr Dir Psychol Sci 25:307–312. https://doi.org/10.1177/0963721416667718
Banerjee K, Chabris CF, Johnson VE et al (2009) General intelligence in another primate: individual differences across cognitive task performance in a new world monkey (Saguinus oedipus). PLoS ONE 4:e5883. https://doi.org/10.1371/journal.pone.0005883
Benson-Amram S, Dantzer B, Stricker G et al (2016) Brain size predicts problem-solving ability in mammalian carnivores. Proc Natl Acad Sci 113:2532–2537. https://doi.org/10.1073/pnas.1505913113
Boogert NJ, Anderson RC, Peters S et al (2011) Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim Behav 81:1209–1216. https://doi.org/10.1016/j.anbehav.2011.03.004
Bray EE, MacLean EL, Hare BA (2014) Context specificity of inhibitory control in dogs. Anim Cogn 17:15–31. https://doi.org/10.1007/s10071-013-0633-z
Bronson RT (1979) Brain weight-body weight scaling in breeds of dogs and cats. Brain Behav Evol 16:227–236. https://doi.org/10.1159/000121839
Carpenter PA, Just MA, Shell P (1990) What one intelligence test measures: a theoretical account of the processing in the Raven progressive matrices test. Psychol Rev 97:404–431. https://doi.org/10.1037/0033-295X.97.3.404
Carreira LM (2016) Using Bronson equation to accurately predict the dog brain weight based on body weight parameter. Vet Sci 3:25–27. https://doi.org/10.3390/vetsci3040036
Cieri RL, Churchill SE, Franciscus RG et al (2014) Craniofacial feminization, social tolerance, and the origins of behavioral modernity. Curr Anthropol 55:419–443. https://doi.org/10.1086/677209
Cole EF, Morand-Ferron J, Hinks AE, Quinn JL (2012) Cognitive ability influences reproductive life history variation in the wild. Curr Biol 22:1808–1812. https://doi.org/10.1016/j.cub.2012.07.051
Croston R, Branch CL, Kozlovsky DY et al (2015) Heritability and the evolution of cognitive traits. Behav Ecol 26:1447–1459. https://doi.org/10.1093/beheco/arv088
Cummins DD, Cummins R (1999) Biological preparedness and evolutionary explanation. Cognition 73:37–53
Darwin C (1859) On the origin of species by means of natural selection, or preservation of favoured races in the struggle for life. John Murray, London
Davidson MC, Amso D, Anderson LC, Diamond A (2006) Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia 44:2037–2078. https://doi.org/10.1016/j.neuropsychologia.2006.02.006
Davies G, Tenesa A, Payton A et al (2011) Genome-wide association studies establish that human intelligence is highly heritable and polygenic. Mol Psychiatry 16:996–1005. https://doi.org/10.1038/mp.2011.85
Deary IJ, Johnson W, Houlihan LM (2009) Genetic foundations of human intelligence. Hum Genet 126:215–232. https://doi.org/10.1007/s00439-009-0655-4
Deary IJ, Penke L, Johnson W (2010) The neuroscience of human intelligence differences. Nat Rev Neurosci 11:201–211. https://doi.org/10.1038/nrn2793
Dorey NR, Udell MAR, Wynne CDL (2009) Breed differences in dogs sensitivity to human points: a meta-analysis. Behav Processes 81:409–415. https://doi.org/10.1016/j.beproc.2009.03.011
Drent PJ, Van Oers K, Van Noordwijk AJ (2003) Realized heritability of personalities in the great tit (Parus major). Proc R Soc B Biol Sci 270:45–51. https://doi.org/10.1098/rspb.2002.2168
Dukas R (2004) Evolutionary biology of animal cognition. Annu Rev Ecol Evol Syst 35:347–374. https://doi.org/10.1146/annurev.ecolsys.35.112202.130152
Frank H, Frank MG (1982) Comparison of problem-solving performance in six-week-old wolves and dogs. Anim Behav 30:95–98. https://doi.org/10.1016/S0003-3472(82)80241-8
Galsworthy MJ, Paya-Cano JL, Liu L et al (2005) Assessing reliability, heritability and general cognitive ability in a battery of cognitive tasks for laboratory mice. Behav Genet 35:675–692. https://doi.org/10.1007/s10519-005-3423-9
Hare B (2017) Survival of the friendliest: homo sapiens evolved via selection for prosociality. Annu Rev Psychol 68:155–186. https://doi.org/10.1146/annurev-psych-010416-044201
Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9:439–444. https://doi.org/10.1016/j.tics.2005.07.003
Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. https://doi.org/10.1126/science.1072702(80-)
Hare B, Rosati A, Kaminski J et al (2010) The domestication hypothesis for dogs’ skills with human communication: a response to Udell et al. (2008) and Wynne al. (2008). Anim Behav 79:1–6. https://doi.org/10.1016/j.anbehav.2009.06.031
Harman HH, Jones WH (1966) Factor analysis by minimizing residuals (minres). Psychometrika 31:351–368
Hart BL, Hart LA (1985) Selecting pet dogs on the basis of cluster analysis of breed behavior profiles and gender. J Am Vet Med Assoc 186:1181–1185
Hart BL, Miller MF (1985) Behavioral profiles of dog breeds. J Am Vet Med Assoc 186:1175–1180
Hayward JJ, Castelhano MG, Oliveira KC et al (2016a) Complex disease and phenotype mapping in the domestic dog. Nat Commun 7:10460. https://doi.org/10.1038/ncomms10460
Hayward JJ, Castelhano MG, Oliveira KC et al (2016b) Data from: complex disease and phenotype mapping in the domestic dog. https://doi.org/10.5061/dryad.266k4
Heberlein MTE, Turner DC, Manser MB (2017) Dogs ’ (Canis familiaris) attention to human perception: influence of breed groups and life experiences. J Comp Psychol 131:19–29
Herculano-Houzel S (2017) Numbers of neurons as biological correlates of cognitive capability. Curr Opin Behav Sci 16:1–7. https://doi.org/10.1016/j.cobeha.2017.02.004
Herrmann E, Call J, Hernandez-Lloreda MV et al (2007) Humans have evolved specialised skills of social cognition: the cultural intelligence hypothesis. Science 317:1360–1366. https://doi.org/10.1126/science.1146282(80-)
Herrmann E, Hernández-Lloreda MV, Call J et al (2010) The structure of individual differences in the cognitive abilities of children and chimpanzees. Psychol Sci 21:102–110. https://doi.org/10.1177/0956797609356511
Hiestand L (2011) A comparison of problem-solving and spatial orientation in the wolf (Canis lupus) and dog (Canis familiaris). Behav Genet 41:840–857. https://doi.org/10.1007/s10519-011-9455-4
Hopkins WD, Russell JL, Schaeffer J (2014) Chimpanzee intelligence is heritable. Curr Biol 24:1649–1652. https://doi.org/10.1016/j.cub.2014.05.076
Horschler DJ, MacLean EL (2019) Leveraging brain–body scaling relationships for comparative studies. Anim Cogn 22:1197–1202. https://doi.org/10.1007/s10071-019-01316-8
Horschler DJ, Hare B, Call J et al (2019) Absolute brain size predicts dog breed differences in executive function. Anim Cogn 22:187–198. https://doi.org/10.1007/s10071-018-01234-1
Hsu Y, Serpell JA (2003) Development and validation of a questionnaire for measuring behavior and temperament traits in pet dogs. J Am Vet Med Assoc 223:1293–1300
Jakovcevic A, Elgier AM, Mustaca AE, Bentosela M (2010) Breed differences in dogs’ (Canis familiaris) gaze to the human face. Behav Processes 84:602–607. https://doi.org/10.1016/j.beproc.2010.04.003
Jardim-Messeder D, Lambert K, Noctor S et al (2017) Dogs Have the Most Neurons, Though Not the Largest Brain: Trade-Off between Body Mass and Number of Neurons in the Cerebral Cortex of Large Carnivoran Species. Front Neuroanat 11:1–18. https://doi.org/10.3389/fnana.2017.00118
Johnson-Ulrich L, Holekamp KE (2020) Group size and social rank predict inhibitory control in spotted hyaenas. Anim Behav 160:157–168. https://doi.org/10.1016/j.anbehav.2019.11.020
Kang HM, Zaitlen NA, Wade CM et al (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723. https://doi.org/10.1534/genetics.107.080101
Karlsson EK, Baranowska I, Wade CM et al (2007) Efficient mapping of mendelian traits in dogs through genome-wide association. Nat Genet 39:1321–1328. https://doi.org/10.1038/ng.2007.10
Keagy J, Savard JF, Borgia G (2009) Male satin bowerbird problem-solving ability predicts mating success. Anim Behav 78:809–817. https://doi.org/10.1016/j.anbehav.2009.07.011
Konno A, Romero T, Inoue-Murayama M et al (2016) Dog breed differences in visual communication with humans. PLoS ONE 11:1–14. https://doi.org/10.1371/journal.pone.0164760
Kotrschal A, Rogell B, Bundsen A et al (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23:168–171. https://doi.org/10.1016/j.cub.2012.11.058
Lampe M, Bräuer J, Kaminski J, Virányi Z (2017) The effects of domestication and ontogeny on cognition in dogs and wolves. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-12055-6
Leach HM (2003) Human domestication reconsidered. Curr Anthropol 44:349–368. https://doi.org/10.1086/368119
MacLean EL (2016) Unraveling the evolution of uniquely human cognition. Proc Natl Acad Sci 113:201521270. https://doi.org/10.1073/pnas.1521270113
MacLean EL, Hare B, Nunn CL et al (2014) The evolution of self-control. Proc Natl Acad Sci 111:E2140–E2148. https://doi.org/10.1073/pnas.1323533111
MacLean EL, Herrmann E, Suchindran S, Hare B (2017) Individual differences in cooperative communicative skills are more similar between dogs and humans than chimpanzees. Anim Behav 126:41–51. https://doi.org/10.1016/j.anbehav.2017.01.005
MacLean EL, Snyder-Mackler N, vonHoldt BM, Serpell JA (2019) Highly heritable and functionally relevant breed differences in dog behaviour. Proc R Soc B Biol Sci 286:1–9. https://doi.org/10.1098/rspb.2019.0716
Marshall-Pescini S, Virányi Z, Range F (2015) The effect of domestication on inhibitory control: wolves and dogs compared. PLoS ONE 10:1–16. https://doi.org/10.1371/journal.pone.0118469
Marshall-Pescini S, Frazzi C, Valsecchi P (2016) The effect of training and breed group on problem-solving behaviours in dogs. Anim Cogn 19:571–579. https://doi.org/10.1007/s10071-016-0960-y
Matzel LD, Han YR, Grossman H et al (2003) Individual differences in the expression of a “general” learning ability in mice. J Neurosci 23:6423–6433. https://doi.org/10.1523/JNEUROSCI.23-16-06423.2003
McGreevy PD, Georgevsky D, Carrasco J et al (2013) Dog behavior co-varies with height, bodyweight and skull shape. PLoS ONE 8:e80529. https://doi.org/10.1371/journal.pone.0080529
Mehrkam LR, Wynne CDL (2014) Behavioral differences among breeds of domestic dogs (Canis lupus familiaris): current status of the science. Appl Anim Behav Sci 155:12–27. https://doi.org/10.1016/j.applanim.2014.03.005
Miklósi Á, Kubinyi EE, Topál J et al (2003) A simple reason for a big difference: wolves do not look back at humans, but dogs do. Curr Biol 13:763–766. https://doi.org/10.1016/S0960-9822(03)00263-X
Moll H, Tomasello M (2007) Cooperation and human cognition: the Vygotskian intelligence hypothesis. Philos Trans R Soc Lond B Biol Sci 362:639–648. https://doi.org/10.1098/rstb.2006.2000
Olsen MR (2018) A case for methodological overhaul and increased study of executive function in the domestic dog (Canis lupus familiaris). Anim Cogn. https://doi.org/10.1007/s10071-018-1162-6
Parker HG, Kim LV, Sutter NB et al (2004) Genetic structure of the purebred domestic dog. Science 304:1160–1164. https://doi.org/10.1126/science.1097406
Parker HG, Dreger DL, Rimbault M et al (2017) Genomic analyses reveal the influence of geographic origin, migration, and hybridization on modern dog breed development. Cell Rep 19:697–708. https://doi.org/10.1016/j.celrep.2017.03.079
Persson ME, Roth LSV, Johnsson M et al (2015) Human-directed social behaviour in dogs shows significant heritability. Genes, Brain Behav 14:337–344. https://doi.org/10.1111/gbb.12194
Polderman TJC, Benyamin B, De Leeuw CA et al (2015) Meta-analysis of the heritability of human traits based on fifty years of twin studies. Nat Genet 47:702–709. https://doi.org/10.1038/ng.3285
Pongrácz P, Miklósi Á, Vida V, Csányi V (2005) The pet dogs ability for learning from a human demonstrator in a detour task is independent from the breed and age. Appl Anim Behav Sci 90:309–323. https://doi.org/10.1016/j.applanim.2004.08.004
Purcell SM, Chang C (2018) PLINK [1.90]. www.cog-genomics.org/plink/1.9/
Purcell SM, Chang CC, Chow CC et al (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4:1–16. https://doi.org/10.1186/s13742-015-0047-8
R Core Team (2018) R: a language and environment for statistical computing. Vienna, Austria. https://www.r-project.org/
Range F, Virányi Z (2015) Tracking the evolutionary origins of dog-human cooperation: the “canine cooperation hypothesis”. Front Psychol 6:1–10. https://doi.org/10.3389/fpsyg.2015.00582
Range F, Jenikejew J, Schröder I, Virányi Z (2014) Difference in quantity discrimination in dogs and wolves. Front Psychol 5:1–10. https://doi.org/10.3389/fpsyg.2014.01299
Revelle W (2018) Psych: procedures for psychological, psychometric, and personality research. Evanston, Illinois. https://cran.r-project.org/package=psych
Riedel J, Schumann K, Kaminski J et al (2008) The early ontogeny of human-dog communication. Anim Behav 75:1003–1014. https://doi.org/10.1016/j.anbehav.2007.08.010
Rosati AG, Rodriguez K, Hare B (2014) The ecology of spatial memory in four lemur species. Anim Cogn. https://doi.org/10.1007/s10071-014-0727-2
Saetre P, Strandberg E, Sundgren PE et al (2006) The genetic contribution to canine personality. Genes, Brain Behav 5:240–248. https://doi.org/10.1111/j.1601-183X.2005.00155.x
Scott JP, Fuller JL (1965) Genetics and the social behavior of the dog. Univ ChicagoPress, Chicago, p 111
Shaw RC, Schmelz M (2017) Cognitive test batteries in animal cognition research: evaluating the past, present and future of comparative psychometrics. Anim Cogn 20:1003–1018. https://doi.org/10.1007/s10071-017-1135-1
Sonnenberg BR, Branch CL, Pitera AM et al (2019) Natural selection and spatial cognition in wild food-caching mountain chickadees. Curr Biol 29:670–676.e3. https://doi.org/10.1016/j.cub.2019.01.006
Stevens J (2002) Applied multivariate statistics for the social sciences. Lawrence Erlbaum Associates, Inc
Stewart L, MacLean EL, Ivy D et al (2015) Citizen science as a new tool in dog cognition research. PLoS ONE 10:1–16. https://doi.org/10.1371/journal.pone.0135176
Sutter NB, Bustamante CD, Chase K et al (2007) A single IGF1 allele is a major determinant of small size in dogs. Science 316:112–115. https://doi.org/10.1126/science.1137045
Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Philos Trans R Soc B Biol Sci 367:2773–2783. https://doi.org/10.1098/rstb.2012.0214
Tomasello M, Call J (2008) Assessing the validity of ape-human comparisons: a reply to Boesch (2007). J Comp Psychol 122:449–452. https://doi.org/10.1037/0735-7036.122.4.449
Tomasello M, Call J (2011) Methodological challenges in the study of primate cognition. Science 334(6060):1227–1228. https://doi.org/10.1126/science.1213443
Udell MAR, Dorey NR, Wynne CDL (2010) What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biol Rev 85:327–345. https://doi.org/10.1111/j.1469-185X.2009.00104.x
Udell MAR, Ewald M, Dorey NR, Wynne CDL (2014) Exploring breed differences in dogs (Canis familiaris): does exaggeration or inhibition of predatory response predict performance on human-guided tasks? Anim Behav 89:99–105. https://doi.org/10.1016/j.anbehav.2013.12.012
Vaysse A, Ratnakumar A, Derrien T et al (2011) Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping. PLoS Genet 7:1–21. https://doi.org/10.1371/journal.pgen.1002316
Virányi Z, Gácsi M, Kubinyi E et al (2008) Comprehension of human pointing gestures in young human-reared wolves (Canis lupus) and dogs (Canis familiaris). Anim Cogn 11:373–387. https://doi.org/10.1007/s10071-007-0127-y
Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9:255–266. https://doi.org/10.1038/nrg2322
VonHoldt BM, Pollinger JP, Lohmueller KE et al (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898–902. https://doi.org/10.1038/nature08837
Watowich MM, MacLean EL, Hare B et al (2020) Age influences domestic dog cognitive performance independent of average breed lifespan. Anim Cogn. https://doi.org/10.1007/s10071-020-01385-0
Willems YE, Boesen N, Li J et al (2019) The heritability of self-control: a meta-analysis. Neurosci Biobehav Rev 100:324–334. https://doi.org/10.1016/j.neubiorev.2019.02.012
Wilmer JB, Germine L, Chabris CF et al (2010) Human face recognition ability is specific and highly heritable. Proc Natl Acad Sci 107:5238–5241. https://doi.org/10.1073/pnas.0913053107
Wilson AJ, Réale D, Clements MN et al (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26. https://doi.org/10.1111/j.1365-2656.2009.01639.x
Wobber V, Hare B, Koler-Matznick J et al (2009) Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals. Interact Stud 10:206–224. https://doi.org/10.1075/is.10.2.06wob
Wynne CDL (2016) What is special about dog cognition? Curr Dir Psychol Sci 25:345–350. https://doi.org/10.1177/0963721416657540
Xavier A, Xu S, Muir W, Rainey K (2015) {NAM}: association studies in multiple populations. Bioinformatics 31:3862–3864
Yeo BTT, Krienen FM, Sepulcre J et al (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106:1125–1165. https://doi.org/10.1152/jn.00338.2011
Zhou X, Stephens M (2012) Genome-wide efficient mixed-model analysis for association studies. Nat Genet 44:821–824. https://doi.org/10.1038/ng.2310
Acknowledgements
We thank David Ivy, Eliot Cohen, Kip Frey, and everyone else who helped create Dognition.com, as well as the members of the advisory board: Josep Call, Juliane Kaminski, Ádám Miklósi, Laurie R. Santos, and Richard Wrangham. We thank Daniel J. Horschler for discussions of the Dognition data and sharing already-tabulated breed-average body weight data, as well as Stacey R. Tecot, Ivy L. Pike, and two anonymous reviewers for comments on previous versions of this manuscript. Lastly, we thank all the dogs and people who participated in Dognition and made this work possible. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. (DGE-1746060). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.
Funding
G.E.G. was funded by the University of Arizona’s University Fellows Program and the NSF Graduate Research Fellowship Program (DGE-1746060). B.H. is supported in part by the National Institute of Health (Grant 1R01HD097732-01).
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The data was collected by citizen scientists through Dognition, with tasks designed by BH. The analysis was primarily designed and conducted by GEG and ELM, with BH and NS-M consulting. The paper was written primarily by GEG with significant contributions and revisions from ELM, BH, and NS-M All authors gave their final approval for publication and agree to be held accountable for the work performed therein.
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BH is a founder of Dognition.com and a member of its Scientific Advisory Board. The authors declare no other competing interests.
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All animals included in this study were pet dogs tested by citizen scientists in their own homes. The use of third-party data from Dognition.com was approved by Duke University IACUC protocol A138-11-06 and data were collected in accordance with relevant guidelines and regulations.
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Genetic data used in these analyses are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.266k4 (Hayward et al. 2016b) and GEO accession nos. GSE90441, GSE83160, GSE70454 and GSE96736. A subset of the Dognition data and the code for our linear mixed models are available at https://github.com/GGnanadesikan/dognition_heritability/. The remaining Dognition data used in these analyses are available from Brian Hare at b.hare@duke.edu.
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Gnanadesikan, G.E., Hare, B., Snyder-Mackler, N. et al. Estimating the heritability of cognitive traits across dog breeds reveals highly heritable inhibitory control and communication factors. Anim Cogn 23, 953–964 (2020). https://doi.org/10.1007/s10071-020-01400-4
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DOI: https://doi.org/10.1007/s10071-020-01400-4