Abstract
The field of animal cognition has advanced rapidly in the last 25 years. Through careful and creative studies of animals in captivity and in the wild, we have gained critical insights into the evolution of intelligence, the cognitive capacities of a diverse array of taxa, and the importance of ecological and social environments, as well as individual variation, in the expression of cognitive abilities. The field of animal cognition, however, is still being influenced by some historical tendencies. For example, primates and birds are still the majority of study species in the field of animal cognition. Studies of diverse taxa improve the generalizability of our results, are critical for testing evolutionary hypotheses, and open new paths for understanding cognition in species with vastly different morphologies. In this paper, we review the current state of knowledge of cognition in mammalian carnivores. We discuss the advantages of studying cognition in Carnivorans and the immense progress that has been made across many cognitive domains in both lab and field studies of carnivores. We also discuss the current constraints that are associated with studying carnivores. Finally, we explore new directions for future research in studies of carnivore cognition.
Similar content being viewed by others
Data availability
The datasets supporting this review article are associated with the original articles that we reference.
References
Aschoff, J, Gunther, B, and Kramer, K (1971). Energiehaushalt und temperaturregulation. Urban and Schwarzenberg.
Audet J-N, Lefebvre L (2017) What’s flexible in behavioral flexibility? Behav Ecol. https://doi.org/10.1093/beheco/arx007
Auersperg AMI, von Bayern AMP, Gajdon GK, Huber L, Kacelnik A (2011) Flexibility in problem solving and tool use of kea and New Caledonian crows in a multi access box paradigm. PLoS ONE 6(6):e20231. https://doi.org/10.1371/journal.pone.0020231
Bailey I, Myatt JP, Wilson AM (2013) Group hunting within the Carnivora: Physiological, cognitive and environmental influences on strategy and cooperation. Behav Ecol Sociobiol 67(1):1–17. https://doi.org/10.1007/s00265-012-1423-3
Barrett LP, Stanton LA, Benson-Amram S (2019) The cognition of ‘nuisance’ species. Anim Behav 147:167–177. https://doi.org/10.1016/j.anbehav.2018.05.005
Bateman PW, Fleming PA (2012) Big city life: Carnivores in urban environments. J Zool 287(1):1–23. https://doi.org/10.1111/j.1469-7998.2011.00887.x
Batt S (2009) Human attitudes towards animals in relation to species similarity to humans: A multivariate approach Bioscience Horizons. Inter J Student Res 2(2):180–190. https://doi.org/10.1093/biohorizons/hzp021
Behrendorff L (2018) Clever girl? An observation of innovative prey handling by a dingo (Canis dingo). Pac Conserv Biol 24(2):194–197. https://doi.org/10.1071/PC17044
Benedict LM, Pitera AM, Branch CL, Kozlovsky DY, Sonnenberg BR, Bridge ES, Pravosudov VV (2020) Elevation-related differences in annual survival of adult food-caching mountain chickadees are consistent with natural selection on spatial cognition. Behav Ecol Sociobiol 74(4):40. https://doi.org/10.1007/s00265-020-2817-2
Bensky MK, Gosling SD, Sinn DL (2013). The world from a dog’s point of view: a review and synthesis of dog cognition research. In: Brockmann HJ, Roper TJ, Naguib M, Mitani JC, Simmons LW, Barrett L (Eds), Advances in the Study of Behavior Academic Press vol. 45: p. 209–406
Benson-Amram S, Holekamp KE (2012) Innovative problem solving by wild spotted hyenas. Proc R Soc b 279(1744):4087–4095. https://doi.org/10.1098/rspb.2012.1450
Benson-Amram S, Heinen VK, Dryer SL, Holekamp KE (2011) Numerical assessment and individual call discrimination by wild spotted hyaenas Crocuta Crocuta. Anim Behav 82(4):743–752. https://doi.org/10.1016/j.anbehav.2011.07.004
Benson-Amram S, Weldele ML, Holekamp KE (2013) A comparison of innovative problem solving between wild and captive spotted hyenas Crocuta Crocuta. Anim Behav 85(2):349–356
Benson-Amram S, Heinen VK, Gessner A, Weldele ML, Holekamp KE (2014) Limited social learning of a novel technical problem by spotted hyenas. Behav Proc 109:111–120. https://doi.org/10.1016/j.beproc.2014.09.019
Benson-Amram S, Dantzer B, Stricker G, Swanson EM, Holekamp KE (2016) Brain size predicts problem-solving ability in mammalian carnivores. Proc Natl Acad Sci 113(9):2532–2537. https://doi.org/10.1073/pnas.1505913113
Benson-Amram S, Gilfillan G, McComb K (2018) Numerical assessment in the wild: Insights from social carnivores. Proc R Soc b 373(1740):20160508. https://doi.org/10.1098/rstb.2016.0508
Bobrowicz K, Osvath M (2018) Cats parallel great apes and corvids in motor self-regulation – not brain but material size matters. Front Psychol 9:1995
Borrego N (2020) Socially tolerant lions (Panthera leo) solve a novel cooperative problem. Anim Cogn 23(2):327–336. https://doi.org/10.1007/s10071-019-01336-4
Borrego N, Dowling B (2016) Lions (Panthera leo) solve, learn, and remember a novel resource acquisition problem. Anim Cogn 19(5):1019–1025. https://doi.org/10.1007/s10071-016-1009-y
Borrego N, Gaines M (2016) Social carnivores outperform asocial carnivores on an innovative problem. Anim Behav 114:21–26. https://doi.org/10.1016/j.anbehav.2016.01.013
Bousquet CAH, Sumpter DJT, Manser MB (2011) Moving calls: A vocal mechanism underlying quorum decisions in cohesive groups. Proc R Soc b 278(1711):1482–1488. https://doi.org/10.1098/rspb.2010.1739
Bräuer J, Bös M, Call J, Tomasello M (2013) Domestic dogs (Canis familiaris) coordinate their actions in a problem-solving task. Anim Cogn 16(2):273–285. https://doi.org/10.1007/s10071-012-0571-1
Bray EE, MacLean EL, Hare BA (2014) Context specificity of inhibitory control in dogs. Anim Cogn 17(1):15–31. https://doi.org/10.1007/s10071-013-0633-z
Brown C, Laland KN (2003) Social learning in fishes A review. Fish Fish 4(3):280–288. https://doi.org/10.1046/j.1467-2979.2003.00122.x
Brubaker L, Dasgupta S, Bhattacherjee D, Bhadra A, Udell M (2017) Differences in problem-solving between canid populations: do domestication and lifetime experience affect persistence? Anim Cogn 20(4):717–723
Brucks D, Marshall-Pescini S, Range F (2019) Dogs and wolves do not differ in their inhibitory control abilities in a non-social test battery. Anim Cogn 22(1):1–15. https://doi.org/10.1007/s10071-018-1216-9
Buechel SD, Boussard A, Kotrschal A, van der Bijl W, Kolm N (2018) Brain size affects performance in a reversal-learning test. Proc R Soc b 285(1871):20172031. https://doi.org/10.1098/rspb.2017.20310
Byrne RW, Corp N (2004) Neocortex size predicts deception rate in primates proceedings of the royal society of London series B biological sciences. https://doi.org/10.1098/rspb.2004.2780
Cadenasso ML, Pickett STA, Schwarz K (2007) Spatial heterogeneity in urban ecosystems: reconceptualizing land cover and a framework for classification. Front Ecol Environ 5:80–88. https://doi.org/10.1890/1540-9295(2007)5[80:SHIUER]2.0.CO;2
Carbone C, Teacher A, Rowcliffe JM (2007) The costs of carnivory. PLoS Biol 5(2):e22. https://doi.org/10.1371/journal.pbio.0050022
Gittleman JL (1989) Carnivore behavior ecology and evolution. SprInger. https://doi.org/10.1007/978-1-4757-4716-4
Casey C, Charrier I, Mathevon N, Reichmuth C (2015) Rival assessment among northern elephant seals: Evidence of associative learning during male–male contests. R Soc Open Sci 2(8):150228. https://doi.org/10.1098/rsos.150228
Chacha J, Szenczi P, González D, Martínez-Byer S, Hudson R, Bánszegi O (2020) Revisiting more or less: Influence of numerosity and size on potential prey choice in the domestic cat. Anim Cogn 23(3):491–501. https://doi.org/10.1007/s10071-020-01351-w
Chambers HR, Heldstab SA, O’Hara SJ (2021) Why big brains? A comparison of models for both primate and carnivore brain size evolution. PLoS ONE 16(12):e0261185. https://doi.org/10.1371/journal.pone.0261185
Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19(21):R995–R1008. https://doi.org/10.1016/j.cub.2009.08.023
Clutton-Brock TH, Brotherton PNM, O’Riain MJ, Griffin AS, Gaynor D, Kansky R, Sharpe L, McIlrath GM (2001) Contributions to cooperative rearing in meerkats. Anim Behav 61(4):705–710. https://doi.org/10.1006/anbe.2000.1631
Cook PF, Reichmuth C, Rouse AA, Libby LA, Dennison SE, Carmichael OT, Kruse-Elliott KT, Bloom J, Singh B, Fravel VA, Barbosa L, Stuppino JJ, Van Bonn WG, Gulland FMD, Ranganath C (2015) Algal toxin impairs sea lion memory and hippocampal connectivity, with implications for strandings. Science 350(6267):1545–1547. https://doi.org/10.1126/science.aac5675
Corral-López A, Bloch NI, Kotrschal A, van der Bijl W, Buechel SD, Mank JE, Kolm N (2017) Female brain size affects the assessment of male attractiveness during mate choice. Sci Adv 3(3):e1601990. https://doi.org/10.1126/sciadv.1601990
Daniels SE, Fanelli RE, Gilbert A, Benson-Amram S (2019) Behavioral flexibility of a generalist carnivore. Anim Cogn 22(3):387–396. https://doi.org/10.1007/s10071-019-01252-7
DeCasien AR, Williams SA, Higham JP (2017) Primate brain size is predicted by diet but not sociality. Nature Ecol Evolution 1(5):1–7. https://doi.org/10.1038/s41559-017-0112
Deecke VB (2012) Tool-use in the brown bear (Ursus arctos). Anim Cogn 15(4):725–730. https://doi.org/10.1007/s10071-012-0475-0
Dickman AJ (2012) From cheetahs to chimpanzees: a comparative review of the drivers of human–carnivore conflict and human-primate conflict. Folia Primatol 83(3–6):377–387. https://doi.org/10.1159/000339812
Doty BA, Combs WC (1969) Reversal learning of object and positional discriminations by mink, ferrets and skunks. Quart J Exper Psychol 21(1):58–62. https://doi.org/10.1080/14640746908400195
Drea CM, Carter AN (2009) Cooperative problem solving in a social carnivore. Anim Behav 78(4):967–977. https://doi.org/10.1016/j.anbehav.2009.06.030
Dror S, Miklósi Á, Sommese A, Temesi A, Fugazza C (2021) Acquisition and long-term memory of object names in a sample of Gifted Word Learner dogs. R Soc Open Sci 8(10):210976. https://doi.org/10.1098/rsos.210976
Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317(5843):1344–1347. https://doi.org/10.1126/science.1145463
Elbroch LM, Levy M, Lubell M, Quigley H, Caragiulo A (2017) Adaptive social strategies in a solitary carnivore. Sci Adv 3(10):e1701218. https://doi.org/10.1126/sciadv.1701218
Endo H, Yamagiwa D, Hayashi Y, Koie H, Yamaya Y, Kimura J (1999) Role of the giant panda’s ‘pseudo-thumb.’ Nature 397(6717):309–310. https://doi.org/10.1038/16830
Engh AL, Esch K, Smale L, Holekamp KE (2000) Mechanisms of maternal rank ‘inheritance’ in the spotted hyaena Crocuta Crocuta. Anim Behav 60(3):323–332. https://doi.org/10.1006/anbe.2000.1502
Engh AL, Siebert ER, Greenberg DA, Holekamp KE (2005) Patterns of alliance formation and post-conflict aggression indicate spotted hyaenas recognize third-party relationships. Anim Behav 69(1):209–217. https://doi.org/10.1016/j.anbehav.2004.04.013
Expósito-Granados M, Castro A, Lozano J, Aznar-Sánchez JA, Carter Requena-Mullor JM, Malo AF, Olszańska A, Morales-Reyes Z, Moleón M, Sánchez-Zapata JA, Cortés-Avizanda A, Fischer J, Martín-López B (2019) Human–carnivore relations: conflicts, tolerance and coexistence in the american west. Enviro Res Letter. https://doi.org/10.1088/1748-9326/ab5485
Feldhamer GA, Drickamer LC, Vessey SH et al (2015) Chapter 17: Carnivora. Mammalogy: adaptation, diversity, ecology, 4th edn. Johns Hopkins University Press, Baltimore, MD, pp 352–373
Fidino M, Herr SW, Magle SB (2018) Assessing online opinions of wildlife through social media. Hum Dimens Wildl 23(5):482–490. https://doi.org/10.1080/10871209.2018.1468943
Foley NM, Springer MS, Teeling EC (2016) Mammal madness: is the mammal tree of life not yet resolved? Phil Trans R Soc B 371:20150140. https://doi.org/10.1098/rstb.2015.0140
Frank H, Frank MG (1982) Comparison of problem-solving performance in six-week-old wolves and dogs. Anim Behav 30(1):95–98. https://doi.org/10.1016/S0003-3472(82)80241-8
Franz M, Nunn CL (2009) Network-based diffusion analysis: A new method for detecting social learning. Proc R Soc b 276(1663):1829–1836. https://doi.org/10.1098/rspb.2008.1824
Fugazza C, Miklósi Á (2014) Deferred imitation and declarative memory in domestic dogs. Anim Cogn 17(2):237–247. https://doi.org/10.1007/s10071-013-0656-5
Fugazza C, Pogány Á, Miklósi Á (2016) Recall of others’ actions after incidental encoding reveals episodic-like memory in dogs. Curr Biol 26(23):3209–3213. https://doi.org/10.1016/j.cub.2016.09.057
Fugazza C, Andics A, Magyari L, Dror S, Zempléni A, Miklósi Á (2021a) Rapid learning of object names in dogs. Sci Rep 11(1):2222. https://doi.org/10.1038/s41598-021-81699-2
Fugazza C, Dror S, Sommese A, Temesi A, Miklósi Á (2021b) Word learning dogs (Canis familiaris) provide an animal model for studying exceptional performance. Sci Rep 11(1):14070. https://doi.org/10.1038/s41598-021-93581-2
Fujii JA, Ralls K, Tinker MT (2015) Ecological drivers of variation in tool-use frequency across sea otter populations. Behav Ecol 26(2):519–526. https://doi.org/10.1093/beheco/aru220
Fujii JA, Ralls K, Tinker MT (2017) Food abundance, prey morphology, and diet specialization influence individual sea otter tool use. Behav Ecol 28(5):1206–1216. https://doi.org/10.1093/beheco/arx011
Fujita K, Morisaki A, Takaoka A, Maeda T, Hori Y (2012) Incidental memory in dogs (Canis familiaris): adaptive behavioral solution at an unexpected memory test. Anim Cogn 15(6):1055–1063. https://doi.org/10.1007/s10071-012-0529-3
Garcia AC, Parsons MA, Young JK (2022) Effects of early-life experience on innovation and problem-solving in captive coyotes. Behav Ecol Sociobiol 76(10):1–12
Gaynor KM, Hojnowski CE, Carter NH, Brashares JS (2018) The influence of human disturbance on wildlife nocturnality. Science 360(6394):1232–1235. https://doi.org/10.1126/science.aar7121
Gehrt S (2003) Raccoon, Procyon lotor and allies. In: Feldhamer G, Thompson B, Chapman J (eds) Wild Mammals of North America. The Johns Hopkins University Press, pp 611–634
Gehrt SD, Gergits WF, Fritzell EK (2008) Behavioral and genetic aspects of male social groups in raccoons. J Mammal 89(6):1473–1480. https://doi.org/10.1644/07-MAMM-A-403.1
Gisiner RC (1985) Male territorial and reproductive behavior in the Steller sea lion, Eumetopias Jubatus (California, Alaska) [Ph.D. University of California, Santa Cruz]. https://www.proquest.com/docview/303363980/abstract/F347C12DCD934ABDPQ/1
Gittleman JL (1986) Carnivore brain size, behavioral ecology, and phylogeny. J Mammal 67(1):23–36. https://doi.org/10.2307/1380998
Gittleman JL (1991) Carnivore olfactory bulb size: Allometry, phylogeny and ecology. J Zool 225(2):253–272. https://doi.org/10.1111/j.1469-7998.1991.tb03815.x
Gnanadesikan GE, Hare B, Snyder-Mackler N, MacLean EL (2020) Estimating the heritability of cognitive traits across dog breeds reveals highly heritable inhibitory control and communication factors. Anim Cogn 23(5):953–964. https://doi.org/10.1007/s10071-020-01400-4
Gompper ME (1996) Sociality and asociality in white-nosed coatis (Nasua narica): Foraging costs and benefits. Behav Ecol 7(3):254–263. https://doi.org/10.1093/beheco/7.3.254
Goodwin GP, Benforado A (2015) Judging the goring ox: Retribution directed toward animals. Cogn Sci 39(3):619–646. https://doi.org/10.1111/cogs.12175
Gorman ML, Mills MG, Raath JP, Speakman JR (1998) High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391(6666):479–481. https://doi.org/10.1038/35131
Gossette RL, Kraus G, Speiss J (1968) Comparison of successive discrimination reversal (SDR) performances of seven mammalian species on a spatial task. Psychonomic Science 12(5):193–194. https://doi.org/10.3758/BF03331265
Goumas M, Lee VE, Boogert NJ, Kelley LA, Thornton A (2020) The role of animal cognition in human–wildlife interactions. Front Psychol 11:3019. https://doi.org/10.3389/fpsyg.2020.589978
Greenberg JR, Holekamp KE (2017) Human disturbance affects personality development in a wild carnivore. Anim Behav 132:303–312. https://doi.org/10.1016/j.anbehav.2017.08.023
Greggor AL, Berger-Tal O, Blumstein DT (2020) The rules of attraction: The necessary role of animal cognition in explaining conservation failures and successes. Annu Rev Ecol Evol Syst 51(1):483–503. https://doi.org/10.1146/annurev-ecolsys-011720-103212
Griebling HJ, Sluka CM, Stanton LA, Barrett LP, Bastos JB, Benson-Amram S (2022) How technology can advance the study of animal cognition in the wild. Curr Opin Behav Sci 45:101120. https://doi.org/10.1016/j.cobeha.2022.101120
Griffin AS, Guez D (2014) Innovation and problem solving: A review of common mechanisms. Behav Proc 109:121–134. https://doi.org/10.1016/j.beproc.2014.08.027
Griffin AS, Netto K, Peneaux C (2017) Neophilia, innovation and learning in an urbanized world: A critical evaluation of mixed findings. Curr Opin Behav Sci 16:15–22. https://doi.org/10.1016/j.cobeha.2017.01.004
Hall KRL, Schaller GB (1964) Tool-using behavior of the California sea otter. J Mammal 45(2):287–298. https://doi.org/10.2307/1376994
Hassanin A, Veron G, Ropiquet A et al (2021) Evolutionary history of Carnivora (Mammalia, Laurasiatheria) inferred from mitochondrial genomes. PLoS ONE 16:e0240770. https://doi.org/10.1371/journal.pone.0240770
Healy SD, Rowe C (2013) Costs and benefits of evolving a larger brain: Doubts over the evidence that large brains lead to better cognition. Anim Behav 86(4):e1–e3. https://doi.org/10.1016/j.anbehav.2013.05.017
Heinsohn R, Packer C (1995) Complex cooperative strategies in group-territorial African lions. Science 269(5228):1260–1262. https://doi.org/10.1126/science.7652573
Herculano-Houzel S (2014) The glia/neuron ratio: How it varies uniformly across brain structures and species and what that means for brain physiology and evolution. Glia 62(9):1377–1391. https://doi.org/10.1002/glia.22683
Hiestand NL (1989) A comparison of problem-solving and spatial orientation in the wolf (Canis lupus) and dog (Canis familiaris) [Ph.D University of Connecticut]. https://www.proquest.com/docview/303752550/abstract/A240DAD1E0514E5CPQ/1
Hilborn A, Pettorelli N, Caro T, Kelly MJ, Laurenson MK, Durant SM (2018) Cheetahs modify their prey handling behavior depending on risks from top predators. Behav Ecol Sociobiol 72(4):74. https://doi.org/10.1007/s00265-018-2481-y
Hirsch BT, Prange S, Hauver SA, Gehrt SD (2013a) Genetic relatedness does not predict racoon social network structure. Anim Behav 85(2):463–470. https://doi.org/10.1016/j.anbehav.2012.12.011
Hirsch BT, Prange S, Hauver SA, Gehrt SD (2013b) Raccoon social networks and the potential for disease transmission. PLoS ONE 8(10):e75830. https://doi.org/10.1371/journal.pone.0075830
Holekamp KE (2007) Questioning the social intelligence hypothesis. Trends Cogn Sci 11(2):65–69. https://doi.org/10.1016/j.tics.2006.11.003
Holekamp KE, Benson-Amram S (2017) The evolution of intelligence in mammalian carnivores. Interface Focus 7(3):20160108. https://doi.org/10.1098/rsfs.2016.0108
Holekamp KE, Cooper SM, Katona CI, Berry NA, Frank LG, Smale L (1997) Patterns of association among female spotted hyenas (Crocuta crocuta). J Mammal 78(1):55–64. https://doi.org/10.2307/1382638
Holekamp KE, Boydston EE, Smale L (2000) Group travel in social carnivores. In: Boinski S, Garber P (eds) On the move: How and why animals travel in groups. University of Chicago Press, pp 587–627
Holekamp KE, Dantzer B, Stricker G, Shaw Yoshida KC, Benson-Amram S (2015) Brains, brawn and sociality: a hyaena’s tale. Anim Behav 103:237–248. https://doi.org/10.1016/j.anbehav.2015.01.023
Hoppitt W, Boogert NJ, Laland KN (2010) Detecting social transmission in networks. J Theor Biol 263(4):544–555. https://doi.org/10.1016/j.jtbi.2010.01.004
Hoppitt W, Samson J, Laland KN, Thornton A (2012) Identification of learning mechanisms in a wild meerkat population. PLoS ONE 7(8):e42044. https://doi.org/10.1371/journal.pone.0042044
Hoppitt W, Laland KN (2008) Social processes influencing learning in animals: A review of the evidence. In Advances in the Study of Behavior. Elsevier, Amsterdam. 38:105–165
Horschler DJ, Hare B, Call J, Kaminski J, Miklósi Á, MacLean EL (2019) Absolute brain size predicts dog breed differences in executive function. Anim Cogn 22(2):187–198. https://doi.org/10.1007/s10071-018-01234-1
Hunter JS (2009) Familiarity breeds contempt: Effects of striped skunk color, shape, and abundance on wild carnivore behavior. Behav Ecol 20(6):1315–1322. https://doi.org/10.1093/beheco/arp144
Isler K, van Schaik CP (2009) The expensive brain: A framework for explaining evolutionary changes in brain size. J Hum Evol 57(4):392–400. https://doi.org/10.1016/j.jhevol.2009.04.009
Iwaniuk AN, Whishaw IQ (1999) How skilled are the skilled limb movements of the raccoon (Procyon lotor)? Behav Brain Res 99(1):35–44. https://doi.org/10.1016/S0166-4328(98)00067-9
Jacob J, Kent M, Benson-Amram S, Herculano-Houzel S, Raghanti MA, Ploppert E, Drake J, Hindi B, Natale NR, Daniels S, Fanelli R, Miller A, Landis T, Gilbert A, Johnson S, Lai A, Hyer M, Rzucidlo A, Anchor C, Lambert K (2021) Cytoarchitectural characteristics associated with cognitive flexibility in raccoons. J Comp Neurol 529(14):3375–3388. https://doi.org/10.1002/cne.25197
Jardim-Messeder D, Lambert K, Noctor S, Pestana FM, de Castro Leal ME, Bertelsen MF, Alagaili AN, Mohammad OB, Manger PR, Herculano-Houzel S (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 11:118. https://doi.org/10.3389/fnana.2017.00118
Jelbert SA, Taylor AH, Gray RD (2016) Does absolute brain size really predict self-control? Hand-tracking training improves performance on the A-not-B task. Biol Let 12(2):20150871. https://doi.org/10.1098/rsbl.2015.0871
Johansson M, Ferreira IA, Støen O-G, Frank J, Flykt A (2016) Targeting human fear of large carnivores—Many ideas but few known effects. Biol Cons 201:261–269. https://doi.org/10.1016/j.biocon.2016.07.010
Johnson-Ulrich L, Johnson-Ulrich Z, Holekamp K (2018) Proactive behavior, but not inhibitory control, predicts repeated innovation by spotted hyenas tested with a multi-access box. Anim Cogn 21(3):379–392. https://doi.org/10.1007/s10071-018-1174-2
Johnson-Ulrich L, Benson-Amram S, Holekamp KE (2019) Fitness consequences of innovation in spotted hyenas. Front Ecol Evol 7:443. https://doi.org/10.3389/fevo.2019.00443
Johnson-Ulrich L, Holekamp KE, Hambrick DZ (2020) Innovative problem-solving in wild hyenas is reliable across time and contexts. Sci Rep 10(1):13000. https://doi.org/10.1038/s41598-020-69953-5
Johnson-Ulrich L, Yirga G, Strong RL, Holekamp KE (2021) The effect of urbanization on innovation in spotted hyenas. Anim Cogn 24(5):1027–1038. https://doi.org/10.1007/s10071-021-01494-4
Johnson-Ulrich L, Johnson-Ulrich Z, Holekamp KE (2022) Natural conditions and adaptive functions of problem-solving in the Carnivora. Curr Opin Behav Sci 44:101111. https://doi.org/10.1016/j.cobeha.2022.101111
Kabadayi C, Bobrowicz K, Osvath M (2018) The detour paradigm in animal cognition. Anim Cogn 21(1):21–35. https://doi.org/10.1007/s10071-017-1152-0
Kaminski J, Nitzschner M (2013) Do dogs get the point? a review of dog–human communication ability. Learn Motiv 44(4):294–302. https://doi.org/10.1016/j.lmot.2013.05.001
Kaminski J (2009) Dogs (Canis familiaris) are adapted to receive human communication. In: Berthoz A, Christen Y (eds) Neurobiology of “Umwelt”: how living beings perceive the world. Springer, New York, pp 103–107
Kansky R, Kidd M, Knight AT (2016) A wildlife tolerance model and case study for understanding human wildlife conflicts. Biol Cons 201:137–145. https://doi.org/10.1016/j.biocon.2016.07.002
Kays RW, Gittleman JL (2001) The social organization of the kinkajou Potos flavus (Procyonidae). J Zool 253(4):491–504. https://doi.org/10.1017/S0952836901000450
Kazu RS, Maldonado J, Mota B, Manger PR, Herculano-Houzel S (2014) Cellular scaling rules for the brain of Artiodactyla include a highly folded cortex with few neurons. Front Neuroanat. https://doi.org/10.3389/fnana.2014.00128
Kellert SR (1985) Public perceptions of predators, particularly the wolf and coyote. Biol Cons 31(2):167–189. https://doi.org/10.1016/0006-3207(85)90047-3
Kelley JL, Brown C (2011) Predation risk and decision making in poeciliid prey. In: Evans JP, Pilastro A, Schlupp I (eds) ecology and evolution of poeciliid fishes. The University of Chicago Press, pp 174–184
Khorozyan I, Waltert M (2019) How long do anti-predator interventions remain effective? Patterns, thresholds and uncertainty. R Soc Open Sc 6(9):190826. https://doi.org/10.1098/rsos.190826
Kienle SS, Cacanindin A, Kendall T, Richter B, Ribeiro-French C, Castle L, Lentes G, Costa DP, Mehta RS (2019) Hawaiian monk seals exhibit behavioral flexibility when targeting prey of different size and shape. J Exper Biol. https://doi.org/10.1242/jeb.194985
Klump BC, Major RE, Farine DR et al (2022) Is bin-opening in cockatoos leading to an innovation arms race with humans? Curr Biol 32:R910–R911. https://doi.org/10.1016/j.cub.2022.08.008
Kraft TS, Venkataraman VV, Wallace IJ et al (2021) The energetics of uniquely human subsistence strategies. Science. https://doi.org/10.1126/science.abf0130
Kruuk H, Parish T (1982) Factors affecting population density, group size and territory size of the European badger, Meles meles. J Zool 196(1):31–39. https://doi.org/10.1111/j.1469-7998.1982.tb03492.x
Kudo H, Dunbar RIM (2001) Neocortex size and social network size in primates. Anim Behav 62(4):711–722. https://doi.org/10.1006/anbe.2001.1808
Kummer H, Goodall J, Weiskrantz L (1985) Conditions of innovative behaviour in primates Philosophical Transactions of the Royal Society of London. B BioL Sc 308(1135):203–214. https://doi.org/10.1098/rstb.1985.0020
Ladds Z, Hoppitt W, Boogert NJ (2017) Social learning in otters. Royal Society Open Science 4(8):170489. https://doi.org/10.1098/rsos.170489
Lazzaroni M, Range F, Bernasconi L, Darc L, Holtsch M, Massimei R, Rao A, Marshall-Pescini S (2019) The role of life experience in affecting persistence: a comparative study between free-ranging dogs, pet dogs, and captive pack dogs. PLoS ONE 14(4):e0214806
Lea SEG, Chow PKY, Leaver LA, McLaren IPL (2020) Behavioral flexibility: a review, a model, and some exploratory tests. Learn Behav 48(1):173–187. https://doi.org/10.3758/s13420-020-00421-w
Leach S, Sutton RM, Dhont K, Douglas KM (2021) When is it wrong to eat animals? The relevance of different animal traits and behaviours. Eur J Soc Psychol 51(1):113–123. https://doi.org/10.1002/ejsp.2718
Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63(4):233–246. https://doi.org/10.1159/000076784
Lozano J, Olszańska A, Morales-Reyes Z, Castro AA, Malo AF, Moleón M, Sánchez-Zapata JA, Cortés-Avizanda A, von Wehrden H, Dorresteijn I, Kansky R, Fischer J, Martín-López B (2019) Human–carnivore relations: a systematic review. Biol Cons 237:480–492. https://doi.org/10.1016/j.biocon.2019.07.002
MacDonald SE, Ritvo S (2016) Comparative cognition outside the laboratory. CCBR 11:49–61. https://doi.org/10.3819/ccbr.2016.110003
Byrne RW, Whiten A (eds) (1988) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. Oxford University Press, Oxford
MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Aureli F, Baker JM, Bania AE, Barnard AM, Boogert NJ, Brannon EM, Bray EE, Bray J, Brent LJN, Burkart JM, Call J, Cantlon JF, Cheke LG, Zhao Y (2014) The evolution of self-control. Proc Natl Acad Sci 111(20):E2140–E2148. https://doi.org/10.1073/pnas.1323533111
MacNulty DR, Tallian A, Stahler DR, Smith DW (2014) Influence of group size on the success of wolves hunting bison. PLoS ONE 9(11):e112884. https://doi.org/10.1371/journal.pone.0112884
Mahamane S, Grunig K, Baker J, Young J, Jordan K (2014) Memory-based quantity discrimination in coyotes (Canis latrans). USDA Wildlife Services - Staff Publications. https://digitalcommons.unl.edu/icwdm_usdanwrc/1623
Manfredo MJ, Dayer AA (2004) Concepts for exploring the social aspects of human–wildlife conflict in a global context. Hum Dimens Wildl 9(4):1–20. https://doi.org/10.1080/10871200490505765
Manrique HM, Völter CJ, Call J (2013) Repeated innovation in great apes. Anim Behav 85(1):195–202. https://doi.org/10.1016/j.anbehav.2012.10.026
Marshall-Pescini S, Virányi Z, Range F (2015) The effect of domestication on inhibitory control: wolves and dogs compared. PLoS ONE 10(2):e0118469. https://doi.org/10.1371/journal.pone.0118469
Marshall-Pescini S, Schwarz JFL, Kostelnik I, Virányi Z, Range F (2017) Importance of a species’ socioecology: wolves outperform dogs in a conspecific cooperation task. Proc Natl Acad Sci 114(44):11793–11798. https://doi.org/10.1073/pnas.1709027114
Marzluff JM, Swift KN (2017) Connecting animal and human cognition to conservation. Curr Opin Behav Sci 16:87–92. https://doi.org/10.1016/j.cobeha.2017.04.005
Maust-Mohl M, Fraser J, Morrison R (2012) Wild minds: What people think about animal thinking. Anthrozoös 25(2):133–147. https://doi.org/10.2752/175303712X13316289505224
Mazur R, Seher V (2008) Socially learned foraging behaviour in wild black bears Ursus Americanus. Anim Behav 75(4):1503–1508. https://doi.org/10.1016/j.anbehav.2007.10.027
McGuire MC, Vonk J, Johnson-Ulrich Z (2017) Ambiguous results when using the ambiguous-cue paradigm to assess learning and cognitive bias in gorillas and a black bear. Behav Sci 7(3):51. https://doi.org/10.3390/bs7030051
Mech LD (2009) Possible use of foresight, understanding, and planning by wolves hunting muskoxen. Arctic 60(2):145–149. https://doi.org/10.14430/arctic239
Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TLL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Murphy WJ (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334(6055):521–524. https://doi.org/10.1126/science.1211028
Mersmann D, Tomasello M, Call J, Kaminski J, Taborsky M (2011) Simple mechanisms can explain social learning in domestic dogs (Canis familiaris). Ethology 117(8):675–690. https://doi.org/10.1111/j.1439-0310.2011.01919.x
Michener GR (2004) Hunting techniques and tool use by North American badgers preying on richardson’s ground squirrels. J Mammal 85(5):1019–1027. https://doi.org/10.1644/BNS-102
Miklósi Á, Pongrácz P, Lakatos G, Topál J, Csányi V (2005) A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans. J Comp Psychol 119(2):179–186. https://doi.org/10.1037/0735-7036.119.2.179
Mischel W, Shoda Y, Rodriguez ML (1989) Delay of gratification in children. Science. https://doi.org/10.1126/science.2658056
Mongillo P, Araujo JA, Pitteri E, Carnier P, Adamelli S, Regolin L, Marinelli L (2013) Spatial reversal learning is impaired by age in pet dogs. Age 35(6):2273–2282. https://doi.org/10.1007/s11357-013-9524-0
Morehouse AT, Boyce MS (2017) Troublemaking carnivores: Conflicts with humans in a diverse assemblage of large carnivores. Ecology and Society, 22(3) https://www.jstor.org/stable/26270147
Morehouse AT, Graves TA, Mikle N, Boyce MS (2016) Nature vs Nurture: Evidence for social learning of conflict behaviour in grizzly bears. PLoS ONE. https://doi.org/10.1371/journal.pone.0165425
Morton FB (2021) Do wild raccoons (Procyon lotor) use tools? Anim Cogn 24(3):433–441. https://doi.org/10.1007/s10071-020-01430-y
Mota B, Herculano-Houzel S (2015) Cortical folding scales universally with surface area and thickness, not number of neurons. Science 349(6243):74–77. https://doi.org/10.1126/science.aaa9101
Müller CA, Cant MA (2010) Imitation and traditions in wild banded mongooses. Curr Biol 20(13):1171–1175. https://doi.org/10.1016/j.cub.2010.04.037
Murphy JB, Fernández-Suárez J, Keppie JD, Jeffries TE (2004) Contiguous rather than discrete paleozoic histories for the avalon and meguma terranes based on detrital zircon data. Geology 32(7):585–588. https://doi.org/10.1130/G20351.1
Murray MH, St. Clair, CC, (2015) Individual flexibility in nocturnal activity reduces risk of road mortality for an urban carnivore. Behav Ecol 26(6):1520–1527. https://doi.org/10.1093/beheco/arv102
Nieder A (2020) The adaptive value of numerical competence. Trends Ecol Evol 35(7):605–617. https://doi.org/10.1016/j.tree.2020.02.009
Nieder A (2021) The evolutionary history of brains for numbers. Trends Cogn Sci 25(7):608–621. https://doi.org/10.1016/j.tics.2021.03.012
Noyce KV, Garshelis DL (2014) Follow the leader: Social cues help guide landscape-level movements of American black bears (Ursus americanus). Can J Zool 92(12):1005–1017. https://doi.org/10.1139/cjz-2014-0029
O’Connor VL, Thomas P, Chodorow M, Borrego N (2022) Exploring innovative problem-solving in African lions (Panthera leo) and snow leopards (Panthera uncia). Behav Proc 199:104648. https://doi.org/10.1016/j.beproc.2022.104648
Okujava V, Natishvili T, Mishkin M, Gurashvili T, Chipashvili S, Bagashvili T, Andronikashvili G, Kvernadze G (2005) One-Trial Visual Recognition in Cats 65:205–212
Ostojić L, Clayton NS (2014) Behavioural coordination of dogs in a cooperative problem-solving task with a conspecific and a human partner. Anim Cogn 17(2):445–459. https://doi.org/10.1007/s10071-013-0676-1
Packer C, Scheel D, Pusey AE (1990) Why lions form groups: Food is not enough. Am Nat 136(1):1–19. https://doi.org/10.1086/285079
Parsons MA, Garcia A, Young JK (2022a) Scavenging vs hunting affects behavioral traits of an opportunistic carnivore. PeerJ 10:e13366. https://doi.org/10.7717/peerj.13366
Parsons MA, Newsome TM, Young JK (2022b) The consequences of predators without prey. Front Ecol Environ 20(1):31–39. https://doi.org/10.1002/fee.2419
Perdue BM, Snyder RJ, Zhihe Z, Marr MJ, Maple TL (2011) Sex differences in spatial ability: a test of the range size hypothesis in the order Carnivora. Biol Let 7(3):380–383. https://doi.org/10.1098/rsbl.2010.1116
Pesendorfer MB, Dickerson S, Dragoo JW (2018) Observation of tool use in striped skunks: How community science and social media help document rare natural phenomena. Ecosphere 9(11):e02484. https://doi.org/10.1002/ecs2.2484
Petelle MB, Jacobs PJ, le Roux A (2022) Innovative problem-solving in a small, wild canid. Anim Cogn. https://doi.org/10.1007/s10071-022-01678-6
Petracca LS, Frair JL, Bastille-Rousseau G, Hunt JE, Macdonald DW, Sibanda L, Loveridge AJ (2019) The effectiveness of hazing African lions as a conflict mitigation tool: Implications for carnivore management. Ecosphere 10(12):e02967. https://doi.org/10.1002/ecs2.2967
Pickett STA, Cadenasso ML, Rosi-Marshall EJ et al (2017) Dynamic heterogeneity: a framework to promote ecological integration and hypothesis generation in urban systems. Urban Ecosyst 20:1–14. https://doi.org/10.1007/s11252-016-0574-9
Piotti P, Szabó D, Bognár Z, Egerer A, Hulsbosch P, Carson RS, Kubinyi E (2018) Effect of age on discrimination learning, reversal learning, and cognitive bias in family dogs. Learn Behav 46(4):537–553. https://doi.org/10.3758/s13420-018-0357-7
Pontzer H (2012) Ecological Energetics in Early Homo. Curr Anthropol 53:S346–S358. https://doi.org/10.1086/667402
Pontzer H (2017) The crown joules: energetics, ecology, and evolution in humans and other primates. Evol Anthropol 26:12–24. https://doi.org/10.1002/evan.21513
Powell LE, Isler K, Barton RA (2017) Re-evaluating the link between brain size and behavioural ecology in primates. Phil Trans R Society b 284(1865):20171765. https://doi.org/10.1098/rspb.2017.1765
Prange S, Gehrt SD, Wiggers EP (2004) Influences of anthropogenic resources on raccoon (Procyon lotor) movements and spatial distribution. J Mammal 85(3):8
Proppe DS, McMillan N, Congdon JV, Sturdy CB (2017) Mitigating road impacts on animals through learning principles. Anim Cogn 20(1):19–31. https://doi.org/10.1007/s10071-016-0989-y
Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59(9):779–791. https://doi.org/10.1525/bio.2009.59.9.9
Rasolofoniaina B, Kappeler PM, Fichtel C (2021a) Wild narrow-striped mongooses use social information to enhance behavioural flexibility. Ethology 127(3):253–266. https://doi.org/10.1111/eth.13123
Rasolofoniaina B, Kappeler PM, Fichtel C (2021b) Neophobia and social facilitation in narrow-striped mongooses. Anim Cogn 24(1):165–175. https://doi.org/10.1007/s10071-020-01429-5
Reader SM, Morand-Ferron J, Flynn E (2016) Animal and human innovation: Novel problems and novel solutions. Phil Trans R Society b 371(1690):20150182. https://doi.org/10.1098/rstb.2015.0182
Reader SM, MacDonald K (2003) Environmental variability and primate behavioural flexibility. animal innovation. Oxford University Press, Oxford, pp 83–116
Reilly CM, Suraci JP, Smith JA, Wang Y, Wilmers CC (2022) Mesopredators retain their fear of humans across a development gradient. Behav Ecol 33(2):428–435. https://doi.org/10.1093/beheco/arab150
Rivas-Blanco D, Pohl I-M, Dale R, Heberlein MTE, Range F (2020) Wolves and dogs may rely on non-numerical cues in quantity discrimination tasks when given the choice. Front Psychol 11:573317. https://doi.org/10.3389/fpsyg.2020.573317
Romero T, Aureli F (2008) Reciprocity of support in coatis (Nasua nasua). J Comp Psychol 122(1):19–25. https://doi.org/10.1037/0735-7036.122.1.19
Rosati AG (2017) Foraging cognition: reviving the ecological intelligence hypothesis. Trends Cogn Sci 21(9):691–702. https://doi.org/10.1016/j.tics.2017.05.011
Roth G, Dicke U (2005) Evolution of the brain and intelligence. Trends Cogn Sci 9(5):250–257. https://doi.org/10.1016/j.tics.2005.03.005
Saito A, Shinozuka K, Ito Y, Hasegawa T (2019) Domestic cats (Felis catus) discriminate their names from other words. Sci Rep 9(1):5394. https://doi.org/10.1038/s41598-019-40616-4
Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011) Brain size and social complexity: a computed tomography study in hyaenidae. Brain Behav Evol 77(2):91–104. https://doi.org/10.1159/000323849
Saliveros AM, Blyth EC, Easter C, Hume GV, McAusland F, Hoppitt W, Boogert NJ (2020) Learning strategies and long-term memory in Asian short-clawed otters (Aonyx cinereus). Royal Society Open Science 7(11):201215. https://doi.org/10.1098/rsos.201215
Schakner ZA, Blumstein DT (2013) Behavioral biology of marine mammal deterrents: a review and prospectus. Biol Cons 167:380–389. https://doi.org/10.1016/j.biocon.2013.08.024
Schell CJ, Young JK, Lonsdorf EV, Santymire RM, Mateo JM (2018) Parental habituation to human disturbance over time reduces fear of humans in coyote offspring. Ecol Evol 8(24):12965–12980. https://doi.org/10.1002/ece3.4741
Schell CJ, Stanton LA, Young JK, Angeloni LM, Lambert JE, Breck SW, Murray MH (2021) The evolutionary consequences of human–wildlife conflict in cities. Evol Appl 14(1):178–197. https://doi.org/10.1111/eva.13131
Schiefelbein H, Stankowich T (2016) Aversive or attractive? The effects of skunk oil on predator behavior. In: Proceedings of the Vertebrate Pest Conference, 27(27). https://doi.org/10.5070/V427110648
Schmelz M, Duguid S, Bohn M, Völter CJ (2017) Cooperative problem solving in giant otters (Pteronura brasiliensis) and asian small-clawed otters (Aonyx cinerea). Anim Cogn 20(6):1107–1114. https://doi.org/10.1007/s10071-017-1126-2
Schusterman RJ (1966) Serial discrimination-reversal learning with and without errors by the California sea lion. J Exp Anal Behav 9(5):593–600. https://doi.org/10.1901/jeab.1966.9-593
Schusterman RJ, Dawson RG (1968) Barking, dominance, and territoriality in male sea lions. Science 160(3826):434–436. https://doi.org/10.1126/science.160.3826.434
Shettleworth S (2009) Cognition, evolution, and behavior (Second Edition). Oxford University Press
Simmons BL, Sterling J, Watson JC (2014) Species and size-selective predation by raccoons (Procyon lotor) preying on introduced intertidal clams. Can J Zool 92(12):1059–1065. https://doi.org/10.1139/cjz-2014-0108
Slagsvold T, Wiebe KL (2011) Social learning in birds and its role in shaping a foraging niche. Phil Trans R Society b 366(1567):969–977. https://doi.org/10.1098/rstb.2010.0343
Sluka CM, Stanko K, Campbell A, Cáceres J, Panoz-Brown D, Wheeler A, Bradley J, Allen C (2018) Incidental spatial memory in the domestic dog (Canis familiaris). Learn Behav 46(4):513–521. https://doi.org/10.3758/s13420-018-0327-0
Smaers JB, Turner AH, Gómez-Robles A, Sherwood CC (2018) A cerebellar substrate for cognition evolved multiple times independently in mammals. Elife 7:e35696. https://doi.org/10.7554/eLife.35696
Smale LF, LG, and Holekamp, KE, (1993) Ontogeny of dominance in free-living spotted hyaenas: Juvenile rank relations with adult females and immigrant males. Anim Behav 46(3):467–477. https://doi.org/10.1006/anbe.1993.1215
Smeele SQ, Anderson Hansen K, Ortiz ST, Johansson F, Kristensen JH, Larsson J, Siebert U, Wahlberg M (2019) Memory for own behaviour in pinnipeds. Anim Cogn 22(6):947–958. https://doi.org/10.1007/s10071-019-01286-x
Smith JE, Kolowski JM, Graham KE, Dawes SE, Holekamp KE (2008) Social and ecological determinants of fission–fusion dynamics in the spotted hyaena. Anim Behav 76(3):619–636. https://doi.org/10.1016/j.anbehav.2008.05.001
Smith JE, Swanson EM, Reed D, Holekamp KE (2012) Evolution of cooperation among mammalian carnivores and its relevance to hominin evolution. Curr Anthropol 53(S6):S436–S452. https://doi.org/10.1086/667653
Heyes C, Galef B Jr (eds) (1996) Social learning in animals: The roots of culture. Elsevier, New York
Sol D (2009) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Let 5(1):130–133. https://doi.org/10.1098/rsbl.2008.0621
Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63(3):495–502. https://doi.org/10.1006/anbe.2001.1953
Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci 102(15):5460–5465. https://doi.org/10.1073/pnas.0408145102
Soley FG, Alvarado-Díaz I (2011) Prospective thinking in a mustelid? Eira barbara (Carnivora) cache unripe fruits to consume them once ripened. Naturwissenschaften 98(8):693–698. https://doi.org/10.1007/s00114-011-0821-0
St. Clair, CC, Backs, J, Friesen, A, Gangadharan, A, Gilhooly, P, Murray, M, and Pollock, S, (2019) Animal learning may contribute to both problems and solutions for wildlife–train collisions. Phil Trans R Society b 374(1781):20180050. https://doi.org/10.1098/rstb.2018.0050
Stander PE (1992) Cooperative hunting in lions: The role of the individual. Behav Ecol Sociobio. https://doi.org/10.1007/BF00170175
Stankowich T, Haverkamp PJ, Caro T (2014) Ecological drivers of antipredator defenses in carnivores: Evolution of noxious weaponry. Evolution 68(5):1415–1425. https://doi.org/10.1111/evo.12356
Stanton L, Davis E, Johnson S, Gilbert A, Benson-Amram S (2017) 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(6):1147–1152
Stanton LA, Bridge ES, Huizinga J, Johnson SR, Young JK, Benson-Amram S (2021) Variation in reversal learning by three generalist mesocarnivores. Anim Cogn 24:3. https://doi.org/10.1007/s10071-020-01438-4
Stanton LA, Bridge ES, Huizinga J, Benson-Amram S (2022) Environmental, individual and social traits of free-ranging raccoons influence performance in cognitive testing. J Exper Biol 225:jeb243726. https://doi.org/10.1242/jeb.243726
Stanton LA (2020) Experimental investigations of cognition in highly adaptable species [Ph.D., University of Wyoming]. https://www.proquest.com/docview/2493543205/abstract/96C81DDC1BEC4D02PQ/1
Stirling I, Laidre KL, Born EW (2021) Do wild polar bears (Ursus maritimus) use tools when hunting walruses (Odobenus rosmarus)? Arctic 74(2):175–187. https://doi.org/10.14430/arctic72532
Striedter GF (2005) Principles of brain evolution. Sinauer Associates, Sunderland, p 436
Swanson EM, Holekamp KE, Lundrigan BL, Arsznov BM, Sakai ST (2012) Multiple determinants of whole and regional brain volume among terrestrial Carnivorans. PLoS ONE 7(6):e38447. https://doi.org/10.1371/journal.pone.0038447
Takagi S, Saito A, Arahori M, Chijiiwa H, Koyasu H, Nagasawa M, Kikusui T, Fujita K, Kuroshima H (2022) Cats learn the names of their friend cats in their daily lives. Sci Rep 12(1):6155. https://doi.org/10.1038/s41598-022-10261-5
Thornton A (2008a) Variation in contributions to teaching by meerkats. Phil Trans R Society b 275(1644):1745–1751. https://doi.org/10.1098/rspb.2008.0268
Thornton A (2008b) Social learning about novel foods in young meerkats. Anim Behav 76(4):1411–1421. https://doi.org/10.1016/j.anbehav.2008.07.007
Thornton A, Clutton-Brock T (2011) Social learning and the development of individual and group behaviour in mammal societies. Phil Trans R Society b 366(1567):978–987. https://doi.org/10.1098/rstb.2010.0312
Thornton A, Malapert A (2009) Experimental evidence for social transmission of food acquisition techniques in wild meerkats. Anim Behav 78(2):255–264. https://doi.org/10.1016/j.anbehav.2009.04.021
Thornton A, McAuliffe K (2006) Teaching in wild meerkats. Science 313(5784):227–229. https://doi.org/10.1126/science.1128727
Thornton A, Samson J (2012) Innovative problem solving in wild meerkats. Anim Behav 83(6):1459–1468. https://doi.org/10.1016/j.anbehav.2012.03.018
Thornton A, Samson J, Clutton-Brock T (2010) Multi-generational persistence of traditions in neighbouring meerkat groups. Proc R Soc b 277(1700):3623–3629. https://doi.org/10.1098/rspb.2010.0611
United Nations (2018) World Urbanization Prospects: the 2018 revision: key facts (pp. 1–2). United Nations. https://population.un.org/wup/Publications/Files/WUP2018-KeyFacts.pdf
Van Bourg J, Young JK, Alkhalifah R, Brummer S, Johansson E, Morton J, Quintana V, Wynne CDL (2022) Cognitive flexibility and aging in coyotes (Canis latrans). J Comp Psychol 136(1):54–67. https://doi.org/10.1037/com0000307
Vonk J, Jett SE (2018) “Bear-ly” learning: Limits of abstraction in black bear cognition. Animal Behavior and Cognition. 5(1):68–78. https://doi.org/10.26451/abc.05.01.06.2018
Vonk J, Beran MJ (2012) Bears ‘count’ too: Quantity estimation and comparison in black bears Ursus Americanus. Anim Behav 84(1):231–238. https://doi.org/10.1016/j.anbehav.2012.05.001
Wahaj SA, Guse KR, Holekamp KE (2001) Reconciliation in the spotted hyena (Crocuta crocuta). Ethology 107(12):1057–1074. https://doi.org/10.1046/j.1439-0310.2001.00717.x
Walker RH, King AJ, McNutt JW, Jordan NR (2017) Sneeze to leave: African wild dogs (Lycaon pictus) use variable quorum thresholds facilitated by sneezes in collective decisions. Proc R Soc b 284(1862):20170347. https://doi.org/10.1098/rspb.2017.0347
Ward C, Smuts BB (2007) Quantity-based judgments in the domestic dog (Canis lupus familiaris). Anim Cogn 10(1):71–80. https://doi.org/10.1007/s10071-006-0042-7
Waroff AJ, Fanucchi L, Robbins CT, Nelson OL (2017) Tool use, problem-solving, and the display of stereotypic behaviors in the brown bear (Ursus arctos). J Vet Behavio 17:62–68. https://doi.org/10.1016/j.jveb.2016.11.003
Warren JM (1960) Discrimination reversal learning by cats. J Genet Psychol 97(2):317–327. https://doi.org/10.1080/00221325.1960.10534337
Warren JM, Warren HB (1962) Reversal learning by horse and raccoon. J Genet Psychol 100(2):215–220. https://doi.org/10.1080/00221325.1962.10533590
Watson SK, Botting J, Whiten A, van de Waal E (2018) Culture and selective social learning in wild and captive primates. In: Di Paolo LD, Di Vincenzo F, De Petrillo F (eds) Evolution of primate social cognition, vol 5. Springer International Publishing, New York, pp 211–230
Webster MM, Laland KN (2017) Social information use and social learning in non-grouping fishes. Behav Ecol 28(6):1547–1552. https://doi.org/10.1093/beheco/arx121
Wehner R, Fukushi T, Isler K (2007) On being small: brain allometry in ants. Brain Behav Evol 69(3):220–228. https://doi.org/10.1159/000097057
Windell RM, Bailey LL, Young JK, Livieri TM, Eads DA, Breck SW (2022) Improving evaluation of nonlethal tools for carnivore management and conservation: evaluating fladry to protect an endangered species from a generalist mesocarnivore. Anim Conserv 25(1):125–136. https://doi.org/10.1111/acv.12726
Wobber V, Hare B, Koler-Matznick J, Wrangham R, Tomasello M (2009) Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals. Interact Stud 10(2):206–224. https://doi.org/10.1075/is.10.2.06wob
Young JK, Hammill E, Breck SW (2019a) Interactions with humans shape coyote responses to hazing. Sci Rep. https://doi.org/10.1038/s41598-019-56524-6
Young JK, Touzot L, Brummer SP (2019b) Persistence and conspecific observations improve problem-solving abilities of coyotes. PLoS ONE 14(7):e0218778. https://doi.org/10.1371/journal.pone.0218778
Young JK, Coppock DL, Baggio JA, Rood KA, Yirga G (2020) Linking human perceptions and spotted hyena behavior in urban areas of Ethiopia. Animal. https://doi.org/10.3390/ani10122400
Zubiria Perez A, Bone C, Stenhouse G (2021) Simulating multi-scale movement decision-making and learning in a large carnivore using agent-based modelling. Ecol Model 452:109568. https://doi.org/10.1016/j.ecolmodel.2021.109568
Acknowledgements
We would like to thank our funding sources and our universities for their support of our research. We would like to thank all of the authors whose work we have included here. We would like to thank the members of the Animal Behavior and Cognition lab at both the University of Wyoming and the University of British Columbia for their insightful discussions on the cognition of Carnivorans over the years. Finally, we would like to thank Kay Holekamp for her mentorship and for being a pioneer of studies of the behavior and cognition of mammalian carnivores.
Funding
SBA is supported by the University of British Columbia, the Natural Sciences and Engineering Research Council of Canada (DGECR-2022–00333 and RGPIN-2022–03590), and the Canada Foundation for Innovation and the British Columbia Knowledge Development Fund (Project # 42035). HJG is supported by the Special UBC Graduate Scholarship-FRST Doctoral Fellowship #6372. CMS is supported by the National Science Foundation Graduate Research Fellowship and the University of Wyoming Biodiversity Institute Graduate Research Enhancement Grant.
Author information
Authors and Affiliations
Contributions
SBA had the original idea for the article. All authors contributed to the literature search, original writing, and editing of the manuscript. All authors read and approved the final manuscript. CMS collected data and created the figures and supplemental material on meta-analysis methods. All authors contributed to figure design and editing.
Corresponding author
Ethics declarations
Conflict of interest
We have no competing interests.
Ethical approval
No approval of research ethics committees was required for this review article, because we summarized research from the existing literature. All ethical approvals for the work that we have reviewed here can be found in the original articles.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Benson-Amram, S., Griebling, H.J. & Sluka, C.M. The current state of carnivore cognition. Anim Cogn 26, 37–58 (2023). https://doi.org/10.1007/s10071-022-01709-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-022-01709-2