Abstract
Cerebral lateralization, which is often reflected in an individual’s behavioral laterality (e.g., handedness and footedness), may bring animals certain benefits such as enhanced cognitive performance. Although the lateralization–cognition relationship has been widely studied in humans and other animals, current evidence supporting their relationship is ambiguous and warrants additional insights from more studies. Moreover, the lateralization–cognition relationship in non-human animals has been mostly studied in human-reared populations, and investigations of wild populations are particularly scarce. Here, we test the footedness of wild-caught male yellow-bellied tits (Pardaliparus venustulus) and investigate its association with their performance in learning to solve a toothpick-pulling problem and a drawer-opening problem. The tested birds showed an overall trend to gradually spent less time solving the problems, implying that they learned to solve the problems. Left- and right-footed individuals showed no significant differences in the latency to explore the experimental apparatuses and in the proportions that completed and did not complete the tasks. However, the left-footed individuals learned faster than the right-footed individuals in the drawer-opening experiment, indicating a potential cognitive advantage associated with left-footedness. These results contribute to the understanding of the behavioral differences between differently footed individuals and, in particular, the relationship between lateralization and cognitive ability in wild animals.
Similar content being viewed by others
Data availability
The data of this study are available from the corresponding author upon request.
References
Allen LL, Morrison KL, Scott WA, Shinn S, Haltiner AM, Doherty MJ (2018) Differences between stance and foot preference evident in Osprey (Pandion haliaetus) fish holding during movement. Brain Behav 8:e01126. https://doi.org/10.1002/brb3.1126
Aplin LM, Sheldon BC, Morand-Ferron J (2013) Milk bottles revisited: social learning and individual variation in the blue tit, Cyanistes caeruleus. Anim Behav 85:1225–1232. https://doi.org/10.1016/j.anbehav.2013.03.009
Baciadonna L, Zucca P, Samour J (2022) Laterality preferences at rest and predatory behaviour of the Gyrfalcon (Falco rusticolus): an alpha predator of the sky. Laterality 27:86–100. https://doi.org/10.1080/1357650X.2021.1958831
Bibost AL, Brown C (2014) Laterality influences cognitive performance in rainbowfish Melanotaenia duboulayi. Anim Cogn 17:1045–1051. https://doi.org/10.1007/s10071-014-0734-3
Bisazza A, Pignatti R, Vallortigara G (1997) Laterality in detour behaviour: interspecific variation in poeciliid fish. Anim Behav 54:1273–1281. https://doi.org/10.1006/anbe.1997.0522
Bluff LA, Troscianko J, Weir AA, Kacelnik A, Rutz C (2010) Tool use by wild New Caledonian crows Corvus moneduloides at natural foraging sites. Proc R Soc B 277:1377–1385. https://doi.org/10.1098/rspb.2009.1953
Brodin A, Utku Urhan A (2015) Sex differences in learning ability in a common songbird, the great tit—females are better observational learners than males. Behav Ecol Sociobiol 69:237–241. https://doi.org/10.1007/s00265-014-1836-2
Brown C, Magat M (2011a) Cerebral lateralization determines hand preferences in Australian parrots. Biol Let 7:496–498. https://doi.org/10.1098/rsbl.2010.1121
Brown C, Magat M (2011b) The evolution of lateralized foot use in parrots: a phylogenetic approach. Behav Ecol 22:1201–1208
Chivers DP, McCormick MI, Warren DT, Allan BJM, Ramasamy RA, Arvizu BK, Glue M, Ferrari MCO (2017) Competitive superiority versus predation savvy: the two sides of behavioural lateralization. Anim Behav 130:9–15. https://doi.org/10.1016/j.anbehav.2017.05.006
Christman SD, Propper RE (2001) Superior episodic memory is associated with interhemispheric processing. Neuropsychology 15:607–616. https://doi.org/10.1037/0894-4105.15.4.607
Donati G, Forrester GS (2021) Hindsight 20/20: the future of laterality research. Laterality 26:330–335. https://doi.org/10.1080/1357650X.2021.1876720
Dukas R (1998) Cognitive ecology: the evolutionary ecology of information processing and decision making. University of Chicago Press, Chicago
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
Ecevitoglu A, Soyman E, Canbeyli R, Unal G (2020) Paw preference is associated with behavioural despair and spatial reference memory in male rats. Behav Process 180:104254. https://doi.org/10.1016/j.beproc.2020.104254
Emery NJ (2006) Cognitive ornithology: the evolution of avian intelligence. Phil Trans R Soc B 361:23–43. https://doi.org/10.1098/rstb.2005.1736
Fesl G, Bruhns P, Rau S, Wiesmann M, Ilmberger J, Kegel G, Brueckmann H (2010) Sensitivity and reliability of language laterality assessment with a free reversed association task—a fMRI study. Eur Radiol 20:683–695. https://doi.org/10.1007/s00330-009-1602-4
Frasnelli E (2013) Brain and behavioral lateralization in invertebrates. Front Psychol 4:939. https://doi.org/10.3389/fpsyg.2013.00939
Frasnelli E, Vallortigara G (2018) Individual-level and population-level lateralization: two sides of the same coin. Symmetry 10:739. https://doi.org/10.3390/sym10120739
Frasnelli E, Vallortigara G, Rogers LJ (2012) Left-right asymmetries of behaviour and nervous system in invertebrates. Biobehav R 36:1273–1291. https://doi.org/10.1016/j.neubiorev.2012.02.006
Gibb J, Hartley PHT (1957) Bird foods and feeding-habits as subjects for amateur research. Br Birds 50:278–291
Gosler A, Clement P (2020) Yellow-bellied Tit Periparus venustulus. In: del Hoyo J, Elliott A, Sargatal J, Christie D (eds) Birds of the Wold. Cornell Lab of Ornithology, Ithaca
Güntürkün O (2005) The avian ‘prefrontal cortex’and cognition. Curr Opin Neurobiol 15:686–693. https://doi.org/10.1016/j.conb.2005.10.003
Guzzetti S, Daini R (2014) Inter-hemispheric recruitment as a function of task complexity, age and cognitive reserve. Aging Neuropsychol C 21:722–745. https://doi.org/10.1080/13825585.2013.874522
Halpern DF, Haviland MG, Killian CD (1998) Handedness and sex differences in intelligence: evidence from the medical college admission test. Brain Cogn 38:87–101. https://doi.org/10.1006/brcg.1998.1021
Herold C, Palomero-Gallagher N, Hellmann B, Kröner S, Theiss C, Güntürkün O, Zilles K (2011) The receptor architecture of the pigeons’ nidopallium caudolaterale: an avian analogue to the mammalian prefrontal cortex. Brain Struct Funct 216:239–254. https://doi.org/10.1007/s00429-011-0301-5
Hook-Costigan MA, Rogers LJ (1998) Eye preferences in common marmosets (Callithrix jacchus): influence of age, stimulus, and hand preference. Laterality 3:109–130. https://doi.org/10.1080/713754297
Hopkins WD, Bennett AJ (1994) Handedness and approach-avoidance behavior in chipanzees (Pan). J Exp Psychol Anim B 20:413–418. https://doi.org/10.1037/0097-7403.20.4.413
Hopkins WD, Washburn DA, Berke L, Williams M (1992) Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a dissociation between hand preference and skill. J Comp Psychol 106:392–397. https://doi.org/10.1037/0735-7036.106.4.392
Hörster W, Ettlinger G (1985) An association between hand preference and tactile discrimination performance in the rhesus monkey. Neuropsychologia 23:411–413. https://doi.org/10.1016/0028-3932(85)90027-2
Isparta S, Salgirli Demirbas Y, Bars Z, Cinar Kul B, Güntürkün O, Ocklenburg S, Da Graca PG (2020) The relationship between problem-solving ability and laterality in cats. Behav Brain Res 391:112691. https://doi.org/10.1016/j.bbr.2020.112691
Izawa E-I, Kusayama T, Watanabe S (2005) Foot-use laterality in the Japanese jungle crow (Corvus macrorhynchos). Behav Process 69:357–362. https://doi.org/10.1016/j.beproc.2005.02.001
Johnsson RD, Brodin A (2019) Wild-caught great tits Parus major fail to use tools in a laboratory experiment, despite facilitation. Ethology 125:324–331. https://doi.org/10.1111/eth.12857
Kaplan G, Rogers LJ (2021) Brain size associated with foot preferences in Australian parrots. Symmetry 13:867. https://doi.org/10.3390/sym13050867
Kozlovsky DY, Branch CL, Pravosudov VV (2015) Problem-solving ability and response to novelty in mountain chickadees (Poecile gambeli) from different elevations. Behav Ecol Sociobiol 69:635–643. https://doi.org/10.1007/s00265-015-1874-4
Leaver LA, Ford S, Miller CW, Yeo MK, Fawcett TW (2020) Learning is negatively associated with strength of left/right paw preference in wild grey squirrels (Sciurus carolinensis). Learn Behav 48:96–103. https://doi.org/10.3758/s13420-019-00408-2
Lucon-Xiccato T, Chivers DP, Mitchell MD, Ferrari MCO (2016) Prenatal exposure to predation affects predator recognition learning via lateralization plasticity. Behav Ecol 28:253–259. https://doi.org/10.1093/beheco/arw155
MacNeilage PF, Rogers LJ, Vallortigara G (2009) Origins of the left and right brain. Sci Am 301:60–67
Magat M, Brown C (2009) Laterality enhances cognition in Australian parrots. Proc R Soc B 276:4155–4162. https://doi.org/10.1098/rspb.2009.1397
Mapp AP, Ono H, Barbeito R (2003) What does the dominant eye dominate? A brief and somewhat contentious review. Percept Psychophys 65:310–317. https://doi.org/10.3758/BF03194802
Martin RJ, Sherry DF (2019) Overwinter temperature has no effect on problem solving abilities or responses to novelty in Black-capped Chickadees (Poecile atricapillus). Behav Process 162:72–78. https://doi.org/10.1016/j.beproc.2019.01.012
McGrew WC, Marchant LF (1999) Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40:509–513. https://doi.org/10.1007/BF02557586
McKeever WF (1986) The influences of handedness, sex, familial sinistrality and androgyny on language laterality, verbal ability, and spatial ability. Cortex 22:521–537. https://doi.org/10.1016/S0010-9452(86)80013-2
Miletto Petrazzini ME, Sovrano VA, Vallortigara G, Messina A (2020) Brain and behavioral asymmetry: a lesson from fish. Front Neuroanat 14:11. https://doi.org/10.3389/fnana.2020.00011
Morand-Ferron J, Cole EF, Quinn JL (2016) Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biol Rev 91:367–389. https://doi.org/10.1111/brv.12174
Niven JE, Bell ATA (2018) Lessons in lateralisation from the insects. Trends Ecol Evol 33:486–488. https://doi.org/10.1016/j.tree.2018.04.008
Ntolka E, Papadatou-Pastou M (2018) Right-handers have negligibly higher IQ scores than left-handers: Systematic review and meta-analyses. Neurosci Biobehav Rev 84:376–393. https://doi.org/10.1016/j.neubiorev.2017.08.007
Ocklenburg S, Berretz G, Packheiser J, Friedrich P (2021) Laterality 2020: Entering the next decade. Laterality 26:265–297. https://doi.org/10.1080/1357650X.2020.1804396
Papadatou-Pastou M (2018) Handedness and cognitive ability: Using meta-analysis to make sense of the data. Prog Brain Res 238:179–206. https://doi.org/10.1016/bs.pbr.2018.06.008
Papp S, Vincze E, Preiszner B, Liker A, Bókony V (2015) A comparison of problem-solving success between urban and rural house sparrows. Behav Ecol Sociobiol 69:471–480. https://doi.org/10.1007/s00265-014-1859-8
Peters M, Reimers S, Manning JT (2006) Hand preference for writing and associations with selected demographic and behavioral variables in 255,100 subjects: the BBC internet study. Brain Cogn 62:177–189. https://doi.org/10.1016/j.bandc.2006.04.005
Preiszner B, Papp S, Pipoly I, Seress G, Vincze E, Liker A, Bókony V (2017) Problem-solving performance and reproductive success of great tits in urban and forest habitats. Anim Cogn 20:53–63. https://doi.org/10.1007/s10071-016-1008-z
Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73:236–253. https://doi.org/10.1006/brln.2000.2305
Rogers LJ (2009) Hand and paw preferences in relation to the lateralized brain. Phil Trans R Soc B 364:943–954. https://doi.org/10.1098/rstb.2008.0225
Rogers LJ (2012) The two hemispheres of the avian brain: their differing roles in perceptual processing and the expression of behavior. J Ornithol 153:S61–S74. https://doi.org/10.1007/s10336-011-0769-z
Rogers LJ (2017) A Matter of degree: strength of brain asymmetry and behaviour. Symmetry 9:57. https://doi.org/10.3390/sym9040057
Rogers LJ (2021) Brain lateralization and cognitive capacity. Animals 11:1996. https://doi.org/10.3390/ani11071996
Rogers LJ, Vallortigara G (2015) When and why did brains break symmetry? Symmetry 7:2181–2194. https://doi.org/10.3390/sym7042181
Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. P Roy Soc Lond B Biol 271:S420–S422. https://doi.org/10.1098/rsbl.2004.0200
Rogers LJ, Vallortigara G, Andrew RJ (2013) Divided brains: the biology and behaviour of brain asymmetries. Cambridge University Press, Cambridge
Romano D, Benelli G, Stefanini C (2017) Escape and surveillance asymmetries in locusts exposed to a Guinea fowl-mimicking robot predator. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-12941-z
Rowe C, Healy SD (2014) Measuring variation in cognition. Behav Ecol 25:1287–1292. https://doi.org/10.1093/beheco/aru090
Shetleworth SJ (2009) Cognition, Evolution, and Behavior, 2nd edn. Oxford University Press, Oxford
Sonnenberg BR, Branch CL, Pitera AM, Bridge E, Pravosudov VV (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
Ströckens F, Güntürkün O, Ocklenburg S (2013) Limb preferences in non-human vertebrates. Laterality 18:536–575. https://doi.org/10.1080/1357650X.2012.723008
Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Phil Trans R Soc B 367:2773–2783
Tommasi L, Vallortigara G (1999) Footedness in binocular and monocular chicks. Laterality 4:89–95. https://doi.org/10.1080/713754325
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589. https://doi.org/10.1017/S0140525X05000105
Vallortigara G, Rogers LJ (2020) A function for the bicameral mind. Cortex 124:274–285. https://doi.org/10.1016/j.cortex.2019.11.018
Vallortigara G, Versace E (2017) Laterality at the Neural, Cognitive, and Behavioral Levels. In: Call J (ed) APA Handbook of Comparative Psychology Basic Concepts, Methods, Neural Substrate, and Behavior, vol 1. American Psychological Association, Washington DC, pp 557–577
Verdolin JL, Harper J (2013) Are shy individuals less behaviorally variable? Insights from a captive population of mouse lemurs. Primates 54:309–314. https://doi.org/10.1007/s10329-013-0360-8
Versace E, Vallortigara G (2015) Forelimb preferences in human beings and other species: multiple models for testing hypotheses on lateralization. Front Psychol 6:233. https://doi.org/10.3389/fpsyg.2015.00233
Vince MA (1964) Use of the feet in feeding by the great tit Parus major. Ibis 106:508–529. https://doi.org/10.1111/j.1474-919X.1964.tb03730.x
Weissman DH, Banich MT (2000) The cerebral hemispheres cooperate to perform complex but not simple tasks. Neuropsychology 14:41–59. https://doi.org/10.1037/0894-4105.14.1.41
Whiteside MA, Bess MM, Frasnelli E, Beardsworth CE, Langley EJG, van Horik JO, Madden JR (2020) No evidence that footedness in pheasants influences cognitive performance in tasks assessing colour discrimination and spatial ability. Learn Behav 48:84–95. https://doi.org/10.3758/s13420-019-00402-8
Yosef R, Gindi C, Sukenik N (2019) Footedness in Steppe buzzards (Buteo vulpinus). Behav Process 158:113–116. https://doi.org/10.1016/j.beproc.2018.11.007
Yu G, Guo J, Xie W, Wang J, Wu Y, Zhang J, Xu J, Li J (2020) Footedness predicts escape performance in a passerine bird. Ecol Evol 10:4251–4260. https://doi.org/10.1002/ece3.6193
Zheng G (2017) A Checklist on the Classification and Distribution of the Birds of China, 3rd edn. Science Press, Beijing
Acknowledgements
We are grateful to Peng Zhang and the staff of the Dongzhai National Nature Reserve for their assistance with bird capturing.
Funding
The project was supported by grants from the National Natural Science Foundation of China (32270520; 31970421).
Author information
Authors and Affiliations
Contributions
JL and JZ conceived the yellow-bellied tit project, JY, JL and GY designed the experiments; JY and GY performed the experiments; JL and YJ analyzed the data and drafted the paper, with all authors contributing to the subsequent revisions. All authors gave final approval for publication and agreed to be held accountable for the work performed therein.
Corresponding author
Ethics declarations
Conflict of interest
We declare we have no competing interests.
Ethical approval
All experimental procedures complied with the current laws of China and were approved by the Ethics and Animal Welfare Committee, Beijing Forestry University (EAWC-BJFU-2020017). Capturing the birds was permitted by Xinyang Forestry Bureau and the Dongzhai National Nature Reserve.
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
Yin, J., Yu, G., Zhang, J. et al. Behavioral laterality is correlated with problem-solving performance in a songbird. Anim Cogn 26, 837–848 (2023). https://doi.org/10.1007/s10071-022-01724-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-022-01724-3