Abstract
Group living can present unique challenges that may require individuals to possess cognitive skills, such as the ability to recognise group members and maintain relationships with specific individuals. These skills may be particularly important for animals that live in large groups, because the intricacies of social life may become more complex when more individuals are involved. Previous research has found that species with regular social interactions tend to show elevated cognitive performance relative to those that rarely interact, yet intraspecific variation in performance among individuals in social groups of varying size is rarely explored. We investigated the relationship between the ability to solve an associative learning task and group size among individuals of a free-living, social bird, the Australian magpie (Cracticus tibicen dorsalis). Individuals varied in their likelihood of interacting with and solving the task. Individuals from larger groups were more likely to approach the associative learning task, suggesting that group size influences individual propensity to attempt a novel task. However, group size did not influence the likelihood that individuals solved the task. Rather, age had an important effect; adults were more likely to solve the association task than juveniles. Our finding that free-living individuals occurring in large social groups were more likely to interact with a novel task suggests that group size may affect differences in performance at a cognitive task within a species.
Similar content being viewed by others
References
Adar E, Lotem A, Barnea A (2008) The effect of social environment on singing behavior in the zebra finch (Taeniopygia guttata) and its implication for neuronal recruitment. Behav Brain Res 187:178–184
Aplin LM, Sheldon BC, Morand-Ferron J (2013) Milk bottles revisited: social learning and individual variation in the blue tit, Cyanistes caeruleu. Anim Behav 85:1225–1232
Baker AM, Mather PB, Hughes JM (2000) Population genetic structure of Australia magpies: evidence for regional differences in juvenile dispersal behaviour. Heredity 85:167–176
Barnea A, Mishal A, Nottebohm F (2006) Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: an anatomical representation of time? Behav Brain Res 167:63–74
Beauchamp G (2010) Group living. In: Breed MD, Moore J (eds) Encyclopedia of animal behaviour. Elsevier, Boston, pp 21–24
Benson-Amram S, Holekamp KE (2012) Innovative problem solving by wild spotted hyenas. Proc R Soc Lond B 279:4087–4095
Benson-Amran S, Weldele ML, Holekamp KE (2013) A comparison of innovative problem-solving abilities between wild and captive spotted hyaenas, Crocuta crocuta. Anim Behav 85:349–356
Biondi LM, Bó MS, Vassallo AI (2010) Inter-individual and age differences in exploration, neophobia and problem-solving ability in a Neotropical raptor (Milvago chimango). Anim Cogn 13:701–710
Blunnel BN, Gore WY, Perkins MN (1980) Performance correlates of social behaviour and organization: social rank and reversal learning in crab-eating macaques (M. fascicularis). Primates 21:376–388
Boeckle M, Bugnyar T (2012) Long-term memory for affiliates in ravens. Curr Biol 22:801–806
Bond AB, Kamil AC, Balda RP (2003) Social complexity and transitive inference in corvids. Anim Behav 65:479–487
Boogert NJ, Anderson RC, Peters S, Searcy WA, Nowicki S (2011) Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim Behav 81:1209–1216
Boogert NJ, Reader SM, Laland KN (2006) The relation between social rank, neophobia and individual learning in starlings. Anim Behav 72:1229–1239
Bouchard J (2002) Is social learning correlated with innovation in birds? An inter-and intraspecific test. Master’s thesis. McGill University, Montreal, Quebec
Brosnan SF, Salwiczek L, Bshary R (2010) The interplay of cognition and cooperation. Proc R Soc Lond B 365:2699–2710
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information- theoretical approach, 2nd edn. Springer-Verlag, New York
Cauchard L, Boogert HJ, Lefebvre L, Dubois F, Doligez B (2013) Problem-solving performance is correlated with reproductive success in a wild bird population. Anim Behav 84:19–26
Cheney DL (2011) Extent and limits of cooperation in animals. Proc Natl Acad Sci U S A 108:10902–10909
Cole EF, Cram DL, Quinn JL (2011) Individual variation in spontaneous problem-solving performance among wild great tits. Anim Behav 81:491–498
Cole EF, Quinn JL (2012) Personality and problem-solving performance explain competitive ability in the wild. Proc R Soc Lond B 279:1168–1175
Croney CC, Newberry RC (2007) Group size and cognitive processes. Appl Anim Behav Sci 103:215–228
Dardenne S, Ducatez S, Cote J, Poncin P, Stevens VM (2013) Neophobia and social tolerance are related to breeding group size in a semi-colonial bird. Behav Ecol Sociobiol 67:1317–1327
Dickinson A (2012) Associative learning and animal cognition. Philos T Roy Soc B 367:2733–2742
Drea CM (1998) Status, age, and sex effects on performance of discrimination tasks in group-tested rhesus monkeys (Macaca mulatta). J Comp Psychol 112:170–183
Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6:178–190
Edwards EK (2014) The impacts of heat on foraging effort and reproductive behaviour in Australian magpies (Cracticus tibicen dorsalis). Honours thesis. University of Western Australia, Australia
Edwards EK, Mitchell NJ, Ridley AR (2015) The impact of high temperatures on foraging behaviour and body condition in the Western Australian magpie Cracticus tibicen dorsalis. Ostrich 86:137–144
Elgar MA (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33
Farabaugh SM, Brown ED, Hughes JM (1992) Cooperative territorial defence in the Australian magpie, Gymnorhina tibicen (Passeriformes, Cracticidae), a group-living songbird. Ethology 92:283–292
Greenberg R (2003) The role of neophobia and neophilia in the development of innovative behaviour. In: Reader SM, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 175–196
Griffin AS, Guez D (2014) Innovation and problem solving: a review of common mechanisms. Behav Process 109:121–134
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711
Gunhold T, Whiten A, Bugnyar T (2014) Video demonstrations seed alternative problem-solving techniques in wild common marmosets. Biol Lett 10:20140439
Hardin JW, Hilbe JM (2013) Generalized estimating equations (GEE), 2nd edn. Taylor and Francis, Hoboken, USA
Hauser MD (1988) How infant vervet monkeys learn to recognize starling alarm calls: the role of experience. Behaviour 105:187–201
Hauser MD (1999) Perseveration, inhibition and the prefrontal cortex: a new look. Curr Opin Neurobiol 9:214–222
Heyes CM, Galef BG Jr (eds) (1996) Social learning in animals: the roots of culture. Academic Press, San Diego
Hopper LM, Price SA, Freeman HD, Lambeth SP, Schapiro SJ, Kendal RL (2014) Influence of personality, age, sex, and estrous state on chimpanzee problem-solving success. Anim Cogn 17:835–847
Hughes JM, Mather PB (1991) Variation in the size of territorial groups in the Australian magpie, Gymnorhina tibicen. Proc R Soc Queensland 101:13–19
Johnstone RE, Storr GM (2004) Handbook of western Australian birds. Western Australian Museum, Perth, Western Australia
Jones DN, Thomas LK (1999) Attacks on humans by Australian magpies: management of an extreme suburban human-wildlife conflict. Wildlife Soc B 27:473–478
Kaplan G (2004) Australian magpie: biology and behaviour of an unusual songbird. CSIRO Publishing, Collingwood, Victoria
Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226
Kendal RL, Coe RL, Laland KN (2005) Age differences in neophilia, exploration, and innovation in family groups of callitrichid monkeys. Am J Primatol 66:167–188
Krause J, Ruxton GD, Krause S (2010) Swarm intelligence in animals and humans. Trends Ecol Evol 25:28–34
Leal M, Powell BJ (2011) Behavioural flexibility and problem-solving in a tropical lizard. Biol Lett 8:28–30
Liker A, Bokony V (2009) Larger groups are more successful in innovative problem solving in house sparrows. Proc Natl Acad Sci U S A 106:7893–7989
Lipkind D, Nottebohm F, Rado R, Barnea A (2002) Social change affects the survival of new neurons in the forebrain of adult songbirds. Behav Brain Res 33:31–34
Majolo B, de Bortoli VA, Schino G (2008) Costs and benefits of group living in primates: group size effects on behaviour and demography. Anim Behav 76:1235–1247
Marshall HH, Carter AJ, Rowcliffe JM, Cowlishaw G (2012) Linking social foraging behaviour with individual time budgets and emergent group-level phenomena. Anim Behav 84:1295–1305
McCormick J (2007) Possible tool use by an Australian magpie (Gymnorhina tibicen). Notornis 54:116–117
Melis AP, Hare B, Tomasello M (2006) Chimpanzees recruit the best collaborators. Science 311:1297–1300
Mirville MO (2013) The effect of group size on the cognitive abilities of the Australian magpie (Cracticus tibicen dorsalis). Honours thesis. University of Western Australia, Australia
Morand-Ferron J, Cole EF, Rawles JEC, Quinn JL (2011) Who are the innovators? A field experiment with two passerine species. Behav Ecol 22:1241–1248
Morand-Ferron J, Hamblin S, Cole EF, Aplin LM, Quinn JL (2015) Taking the operant paradigm into the field: associative learning in wild great tits. PLoS One 10:e0133821
Morand-Ferron J, Quinn JL (2011) Larger groups of passerines are more efficient problem solvers in the wild. Proc Natl Acad Sci U S A 108:5898–15903
Overington SE, Cauchard L, Côté KA, Lefebvre L (2011) Innovative foraging behaviour in birds: what characterizes an innovator? Behav Process 87:274–285
Reader SM, Laland KN (2001) Primate innovation: sex, age and social rank differences. Int J Primatol 22:787–805
Resende BD, Nagy-Reis MB, Lacerda FN, Pagnotta M, Savalli C (2014) Tufted capuchin monkeys (Sapajus sp) learning how to crack nuts: does variability decline throughout development? Behav Process 109:89–94
Ridley AR, Nelson-Flower MJ, Thompson AM (2013) Is sentinel behaviour safe? An experimental investigation. Anim Behav 85:137–142
Ridley AR, Raihani NJ (2007) Facultative response to kleptoparasite by the cooperatively breeding pied babbler. Behav Ecol 18:324–330
Ridley AR, Raihani NJ, Bell MBV (2010) Experimental evidence that sentinel behaviour is affected by risk. Biol Lett 6:445–448
Robinson A (1956) The annual reproductive cycle of the magpie, Gymnorhina dorsalis (Campbell), in south-western Australia. Emu 56:232–336
Rosati AG, Hare B (2012) Decision making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Anim Behav 84:869–879
Rowe C, Healy SD (2014) Measuring variation in cognition. Behav Ecol 25:1287–1292
Sallet J, Mars RB, Noonan MP, Andersson JL, O’Reilly JX, Jbabdi S, Croxson PL, Jenkinson M, Miller KL, Rushmore MFS (2011) Social network size affects neural circuits in macaques. Science 334:697–700
Scace J, Dobberfuhl A, Higgins E, Shumway C (2006) Complexity and the evolution of the social brain. InterJournal, Complex Systems 1844
Sewall KB (2015) Social complexity as a driver of communication and cognition. Integr Comp Biol 55:384–395
Sharpe LL, Joustra AS, Cherry MI (2010) The presence of an avian co-forager reduces vigilance in a cooperative mammal. Biol Lett 6:475–477
Shettleworth SJ (2009) Animal cognition: deconstructing avian insight. Curr Biol 19:R1039–R1040
Silk JB (2007) Social components of fitness in primate groups. Science 317:1347–1351
Sol D, Bacher S, Reader SM, Lefebvre L (2008) Brain size predicts the success of mammal species introduced into novel environments. Am Nat 172:S63–S71
Sorato E, Gullett PR, Griffith SC, Russell AF (2012) Effects of predation risk on foraging behaviour and group size: adaptations in a social cooperative species. Anim Behav 84:823–834
Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21
Thompson AM, Ridley AR (2013) Do fledglings choose wisely? An experimental investigation into social foraging behaviour. Behav Ecol Sociobiol 67:69–78
Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Philos T Roy Soc B 367:2773–2783
Thornton A, McAuliffe K (2015) Cognitive consequences of cooperative breeding? A critical appraisal. J Zool 295:12–22
Thornton A, Samson J (2012) Innovative problem solving in wild meerkats. Anim Behav 83:1459–1468
Thornton A, Isden J, Madden JR (2014) Towards wild psychometrics: linking individual cognitive differences to fitness. Behav Ecol 25:1299–1301
van De Waal E, Bshary R (2010) Contact with human facilities appears to enhance technical skills in wild vervet monkeys (Chlorocebus aethiops). Folia Primatol 81:282–291
van Schaik CP, Isler K, Burkart JM (2012) Explaining brain size variation: from social to cultural brain. Trends Cogn Sci 16:277–284
Weib BM, Scheiber IBR (2013) Long-term memory of hierarchical relationships in free-living graylag geese. Anim Cogn 16:91–97
Acknowledgments
First and foremost, we would like to thank Dr. Eleanor Rowley for not only establishing the magpie population involved in this research, but also sharing her 15 years of knowledge on the magpies to allow research to continue. We would like to thank Alex Thornton, Cyril Grueter and our manuscript reviewers for providing valuable input into the development of the manuscript. Additionally, we would like to thank Ben Ashton and Emily Edwards for their assistance in the field. This research was funded by the School of Animal Biology, University of Western Australia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All observations performed on free-living magpies in this study were in accordance with the ethical standards of the Animal Ethics Committee, University of Western Australia (Approval number RA/100/1272).
Additional information
Communicated by N. Clayton
Significance statement
Research suggests that there is considerable variation in cognitive ability among species from different social settings, yet variation among individuals that differ in sociality is yet to be sufficiently explored. We investigated variation in associative learning among individuals in social groups of varying size in a wild population of magpies, a cooperative bird species. Presenting a colour association foraging task to individuals revealed that individuals from larger groups were more likely to attempt to solve the task. Additionally, older individuals were more successful at solving the task, suggesting that both social and individual differences contribute to associative learning ability. These findings present a significant contribution to understanding cognitive variation among individuals, because social differences, in particular group size, may determine the opportunity that an individual has to acquire the skills and behaviours necessary for overcoming social and ecological challenges.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 129 kb)
Rights and permissions
About this article
Cite this article
Mirville, M.O., Kelley, J.L. & Ridley, A.R. Group size and associative learning in the Australian magpie (Cracticus tibicen dorsalis). Behav Ecol Sociobiol 70, 417–427 (2016). https://doi.org/10.1007/s00265-016-2062-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-016-2062-x