Animal Cognition

, Volume 20, Issue 4, pp 591–602 | Cite as

Neophobia is negatively related to reversal learning ability in females of a generalist bird of prey, the Chimango Caracara, Milvago chimango

  • Jorgelina María Guido
  • Laura Marina BiondiEmail author
  • Aldo Ivan Vasallo
  • Rubén Nestor Muzio
Original Paper


In an ever-changing environment, the ability to adapt choices to new conditions is essential for daily living and ultimately, for survival. Behavioural flexibility allows animals to maximise survival and reproduction in novel settings by adjusting their behaviour based on specific information and feedback acquired in their current environments. However, a growing body of evidence indicates that an individual’s personality type can limit the extent to which the individual might behave flexibly, by influencing the way an individual pays attention to novelty and how much information it collects and stores, which in turn affects the individual’s decision-making and learning process. In this study, the behavioural flexibility of a generalist predator, the Chimango Caracara, Milvago chimango, was analysed using the reversal learning paradigm, focusing on the comparison between age classes, and the relation of learning flexibility with a personality trait, the level of neophobia. Due to the low number of male individuals captured, this study was carried out only with female birds. The results showed that age had no significant effect either on the acquisition of a stimulus-reward association, or on the capacity of reversing this previously learned association. Reversal of the response was a harder task for these birds in comparison with the initial acquisition process. The individual’s performances in the learning tasks seemed to be uncorrelated with each other, suggesting that they involve different neural mechanisms. Contrary to the general pattern observed in the majority of previous work on personality and cognition in non-human animals, the level of neophobia did not correlate with the initial associative learning performance in both adults and juveniles, yet it showed a significant negative relationship with reversal learning ability, mainly in the regressive phase of this task, for the two age classes. Our results suggest that the predatory and generalist lifestyle of female individuals of M. chimango along with the selective pressures of the environment of the individuals studied might play a critical role in the degree and direction of the linkage between novelty response and learning flexibility observed in this study.


Learning Neophobia Behavioral flexibility Chimango Caracara 



We thank Maria Susana Bó and Enrique Madrid for her assistance during the capture and management of raptors and Susana Rosso and Jorge Sanchez for allowing access to their properties to capture birds. We appreciate the improvements in English usage made by Elena Okada. This work was conducted with funds provided by the Grant EXA622/12 from the National University of Mar del Plata, Grant PIP 0893 from the CONICET and by Grant PICT 2243 from FONCYT, Argentina.


  1. Aprile G, Bertonatti C (1996) Manual sobre rehabilitación de fauna. Boletín Técnico FVSA (Fundación Vida Silvestre Argentina), Buenos AiresGoogle Scholar
  2. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus): behavioural syndromes. J Evol Biol 18:464–473. doi: 10.1111/j.1420-9101.2004.00817.x CrossRefPubMedGoogle Scholar
  3. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834. doi: 10.1111/j.1461-0248.2007.01081.x CrossRefPubMedGoogle Scholar
  4. Benus RF, Koolhaas JM, Van Oortmerssen GA (1987) Individual differences in behavioural reaction to a changing environment in mice and rats. Behaviour 100:105–122CrossRefGoogle Scholar
  5. Benus RF, Den Daas S, Koolhaas JM, Van Oortmerssen GA (1990) Routine formation and flexibility in social and non-social behaviour of aggressive and non-aggressive male mice. Behaviour 112:176–193CrossRefGoogle Scholar
  6. Biondi LM, Bó MS, Favero M (2005) Dieta del chimango (Milvago chimango) durante el periodo reproductivo en el sudeste de la provincia de Buenos Aires, Argentina. Ornitol Neotrop 16:31–42Google Scholar
  7. Biondi LM, Bo MS, Vassallo AI (2008) Experimental assessment of problem solving by Milvago chimango (Aves: Falconiformes). J Ethol 26:113–118CrossRefGoogle Scholar
  8. 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 13:701–710CrossRefPubMedGoogle Scholar
  9. Biondi LM, Guido JM, Bó MS et al (2015) The role of stimulus complexity, age and experience in the expression of exploratory behaviour in the Chimango Caracara, Milvago chimango. Anim Cogn 18:139–150CrossRefPubMedGoogle Scholar
  10. Bloom PH (1987) Capturing and handling raptors. In: Giron Pendelton BA, Millsap BA, Cline KW, Bird DM (eds) Raptor management techniques manual. National Wildlife Federation, Washington, pp 99–123Google Scholar
  11. Bolhuis JE, Schouten WG, de Leeuw JA et al (2004) Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav Brain Res 152:351–360CrossRefPubMedGoogle Scholar
  12. Bond AB, Kamil AC, Balda RP (2007) Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica). J Comp Psychol 121:372–379CrossRefPubMedGoogle Scholar
  13. Bontè E, Flemming T, Fagot J (2011) Executive control of perceptual features and abstract relations by baboons (Papio papio). Behav Brain Res 222:176–182CrossRefPubMedGoogle Scholar
  14. Brown C (2012) Experience and learning in changing environments. In: Candolin U, Wong BBM (eds) Behavioral responses to a changing world, 1st edn. Oxford University Press, Oxford, pp 46–60CrossRefGoogle Scholar
  15. Capaldi EJ, Stevenson HW (1957) Reversal following different amounts of training. J Comp Physiol Psychol 50:195–198CrossRefPubMedGoogle Scholar
  16. Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57:491–498CrossRefGoogle Scholar
  17. Chadman KK, Watson DJ, Stanton ME (2006) NMDA receptor antagonism impairs reversal learning in developing rats. Behav Neurosci 120:1071–1083CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chittka L, Skorupski P, Raine NE (2009) Speed–accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407. doi: 10.1016/j.tree.200902.010 CrossRefPubMedGoogle Scholar
  19. Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936CrossRefPubMedGoogle Scholar
  20. Day LB, Crews D, Wilczynski W (1999) Spatial and reversal learning in congeneric lizards with different foraging strategies. Anim Behav 57:393–407CrossRefPubMedGoogle Scholar
  21. Dias R, Robbins TW, Roberts AC (1997) Dissociable forms of inhibitory control within prefrontal cortex with an analogue of the Wisconsin Card Sort Test: restriction to novel situations and independence from “on-line” processing. J Neurosci 17:9285–9297PubMedGoogle Scholar
  22. Dingemanse NJ, Wright J, Kazem AJN et al (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138CrossRefPubMedGoogle Scholar
  23. Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50CrossRefPubMedGoogle Scholar
  24. Dukas R (2009) Learning: mechanisms, ecology, and evolution. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II. University of Chicago Press, Chicago, pp 7–26CrossRefGoogle Scholar
  25. Dukas R (2013) Effects of learning on evolution: robustness, innovation and speciation. Anim Behav 85:1023–1030CrossRefGoogle Scholar
  26. Ferguson-Lees J, Christie DA (2001) Raptors of the world. Houghton Mifflin Harcourt, BostonGoogle Scholar
  27. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  28. Frost AJ, Winrow-Giffen A, Ashley PJ, Sneddon LU (2007) Plasticity in animal personality traits: does prior experience alter the degree of boldness? Proc R Soc Lond B Biol Sci 274:333–339CrossRefGoogle Scholar
  29. Greenberg R (1983) The role of neophobia in determining the degree of foraging specialization in some migrant warblers. Am Nat 122:444–453CrossRefGoogle Scholar
  30. Greenberg R (2003) The role of neophobia and neophilia in the development of innovative behaviour of birds. In: Reader SM, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 175–196CrossRefGoogle Scholar
  31. Greggor AL, Thornton A, Clayton NS (2015) Neophobia is not only avoidance: improving neophobia tests by combining cognition and ecology. Curr Opin Behav Sci 6:82–89. doi: 10.1016/j.cobeha.2015.10.007 CrossRefGoogle Scholar
  32. Griffin AS, Guillette LM, Healy SD (2015) Cognition and personality: an analysis of an emerging field. Trends Ecol Evol 30:207–214. doi: 10.1016/j.tree.2015.01.012 CrossRefPubMedGoogle Scholar
  33. Groothuis TG, Carere C (2005) Avian personalities: characterization and epigenesis. Neurosci Biobehav Rev 29:137–150CrossRefPubMedGoogle Scholar
  34. Gruszka A, Matthews G, Szymura B (2009) Handbook of individual differences in cognition: attention, memory, and executive control. Springer, New YorkGoogle Scholar
  35. Guillette LM, Reddon AR, Hurd PL, Sturdy CB (2009) Exploration of a novel space is associated with individual differences in learning speed in black-capped chickadees, Poecile atricapillus. Behav Process 82:265–270CrossRefGoogle Scholar
  36. Guillette LM, Reddon AR, Hoeschele M, Sturdy CB (2011) Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task. Proc R Soc Lond B Biol Sci 278:767–773. doi: 10.1098/rspb.2010.1669 CrossRefGoogle Scholar
  37. Johnson C, Wilbrecht L (2011) Juvenile mice show greater flexibility in multiple choice reversal learning than adults. Dev Cogn Neurosci 1:540–551. doi: 10.1016/j.dcn.2011.05.008 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kim J, Ragozzino ME (2005) The involvement of the orbitofrontal cortex in learning under changing task contingencies. Neurobiol Learn Mem 83:125–133CrossRefPubMedPubMedCentralGoogle Scholar
  39. Koolhaas JM, De Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307–321CrossRefPubMedGoogle Scholar
  40. LaClair M, Lacreuse A (2016) Reversal learning in gonadectomized marmosets with and without hormone replacement: are males more sensitive to punishment? Anim Cogn 19:619–630CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liedtke J, Schneider JM (2014) Association and reversal learning abilities in a jumping spider. Behav Process 103:192–198. doi: 10.1016/j.beproc.2013.12.015 CrossRefGoogle Scholar
  42. Manrique HM, Call J (2015) Age-dependent cognitive inflexibility in great apes. Anim Behav 102:1–6CrossRefGoogle Scholar
  43. Matzel LD, Han YR, Grossman H et al (2003) Individual differences in the expression of a “general” learning ability in mice. J Neurosci 23:6423–6433PubMedGoogle Scholar
  44. Menzel R (1969) On honey bees memory of spectral colours. 2. Reversal learning and learning of several colours. Z Vgl Physiol 63:290–309CrossRefGoogle Scholar
  45. Mettke-Hofmann C (2014) Cognitive ecology: ecological factors, life-styles, and cognition. Wiley Interdiscip Rev Cogn Sci 5:345–360. doi: 10.1002/wcs.1289 CrossRefPubMedGoogle Scholar
  46. Møller AP (2009) Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849–858. doi: 10.1007/s00442-008-259-8 CrossRefPubMedGoogle Scholar
  47. Mongillo P, Araujo JA, Pitteri E et al (2013) Spatial reversal learning is impaired by age in pet dogs. Age 35:2273–2282. doi: 10.1007/s11357-013-9524-0 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Moore TL, Killiany RJ, Herndon JG, Rosene DL, Moss MB (2003) Impairment in abstraction and set shifting in aged rhesus monkey. Neurobiol Aging 24:125–134CrossRefPubMedGoogle Scholar
  49. Moore TL, Killiany RJ, Herndon JG, Rosene DL, Moss MB (2005) A non-human primate test of abstraction and set shifting: an automated adaptation of the Wisconsin card sorting test. J Neurosci Methods 146:165–173CrossRefPubMedGoogle Scholar
  50. Moore TL, Killiany RJ, Herndon JG, Rosene DL, Moss MB (2006) Executive system dysfunction occurs as early as middle-age in the rhesus monkey. Neurobiol Aging 27:1484–1493CrossRefPubMedGoogle Scholar
  51. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20:831–844. doi: 10.1111/j.1420-9101.2007.01300.x CrossRefPubMedGoogle Scholar
  52. Pagani JH, Brown KL, Stanton ME (2005) Contextual modulation of spatial discrimination reversal in developing rats. Dev Psychobiol 46:36–46CrossRefPubMedGoogle Scholar
  53. Palencia CA, Ragozzino ME (2004) The influence of NMDA receptors in the dorsomedial striatum on response reversal learning. Neurobiol Learn Mem 82:81–89CrossRefPubMedGoogle Scholar
  54. Pavlov IP (1906) The scientific investigation of the psychical faculties or processes in the higher animals. Science 24:613–619CrossRefGoogle Scholar
  55. Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer Science & Business Media, BerlinCrossRefGoogle Scholar
  56. Pubols BHJr (1956) The facilitation of visual and spatial discrimination reversal by overtraining. J Comp Physiol Psychol 49:243–248CrossRefPubMedGoogle Scholar
  57. Ragozzino ME, Detrick S, Kesner RP (1999) Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19:4585–4594PubMedGoogle Scholar
  58. Ragozzino ME, Ragozzino KE, Mizumori SJ, Kesner RP (2002) Role of the dorsomedial striatum in behavioral flexibility for response and visual cue discrimination learning. Behav Neurosci 116:105–115CrossRefPubMedPubMedCentralGoogle Scholar
  59. Range F, Bugnyar T, Schlögl C, Kotrschal K (2006) Individual and sex differences in learning abilities of ravens. Behav Process 73:100–106. doi: 10.1016/j.beproc.2006.04.002 CrossRefGoogle Scholar
  60. Ratcliffe JM, Fenton MB, Shettleworth SJ (2006) Behavioral flexibility positively correlated with relative brain volume in predatory bats. Brain Behav Evol 67:165–176CrossRefPubMedGoogle Scholar
  61. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. 2013. ISBN 3-900051-07-0Google Scholar
  62. Reader SM (2003) Innovation and social learning: individual variation and brain evolution. Anim Biol 53:147–158CrossRefGoogle Scholar
  63. Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci 99:4436–4441CrossRefPubMedPubMedCentralGoogle Scholar
  64. Reader SM, MacDonald K (2003) Environmental variability and primate behavioural flexibility. In: Reader SM, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 83–116CrossRefGoogle Scholar
  65. Réale D, Reader SM, Sol D et al (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  66. Réale D, Dingemanse NJ, Kazem AJ, Wright J (2010) Evolutionary and ecological approaches to the study of personality. Philos Trans R Soc Lond B Biol Sci 365:3937–3946CrossRefPubMedPubMedCentralGoogle Scholar
  67. Rebolo-Ifrán N, Carrete M, Sanz-Aguilar A et al (2015) Links between fear of humans, stress and survival support a non-random distribution of birds among urban and rural habitats. Sci Rep. doi: 10.1038/srep13723 PubMedPubMedCentralGoogle Scholar
  68. Sarasola JH, Negro JJ, Bechard MJ, Lanusse A (2011) Not as similar as thought: sexual dichromatism in Chimango Caracaras is expressed in the exposed skin but not in the plumage. J Ornithol 152:473–479CrossRefGoogle Scholar
  69. Shettleworth SJ (2010) Cognition, evolution, and behavior. Oxford University Press, New YorkGoogle Scholar
  70. Sih A, Del Giudice M (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc Lond B Biol Sci 367:2762–2772. doi: 10.1098/rstb.20120216 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277CrossRefPubMedGoogle Scholar
  72. Sih A, Mathot KJ, Moirón M et al (2015) Animal personality and state–behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60CrossRefPubMedGoogle Scholar
  73. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112CrossRefGoogle Scholar
  74. Sutherland NS, Mackintosh NJ (1971) Mechanisms of animal discrimination learning. Academic Press, New YorkGoogle Scholar
  75. Tebbich S, Stankewitz S, Teschke I (2012) The relationship between foraging, learning abilities and neophobia in two species of Darwin’s finches. Ethology 118:135–146CrossRefGoogle Scholar
  76. Thomson JS, Watts PC, Pottinger TG, Sneddon LU (2012) Plasticity of boldness in rainbow trout, Oncorhynchus mykiss: do hunger and predation influence risk-taking behaviour? Horm Behav 61:750–757CrossRefPubMedGoogle Scholar
  77. Titulaer M, van Oers K, Naguib M (2012) Personality affects learning performance in difficult tasks in a sex-dependent way. Anim Behav 83:723–730CrossRefGoogle Scholar
  78. Verbeek ME, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121CrossRefGoogle Scholar
  79. Watanabe S (2006) The neural basis of cognitive flexibility in birds. In: Wasserman EA, Zentall TR (eds) Comparative cognition: experimental explorations of animal intelligence. Oxford University Press, Oxford, pp 619–639Google Scholar
  80. Weed MR, Bryant R, Perry S (2008) Cognitive development in macaques: attentional set-shifting in juvenile and adult rhesus monkeys. Neuroscience 157:22–28CrossRefPubMedGoogle Scholar
  81. White CM, Olsen PD, Cliff LF (1994) New world vultures to Guineafowl. In: Del Hoyo J, Sargalat EA (eds) Handbook of the birds of the world 2. Lynx Editions, Barcelona, pp 216–247Google Scholar
  82. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall Inc., Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Jorgelina María Guido
    • 1
  • Laura Marina Biondi
    • 2
    Email author
  • Aldo Ivan Vasallo
    • 2
  • Rubén Nestor Muzio
    • 3
  1. 1.Laboratorio Ecotono INIBIOMA (CONICET- Universidad Nacional del Comahue)BarilocheArgentina
  2. 2.Instituto de Investigaciones Marinas y Costeras (IIMyC)CONICET – Universidad Nacional de Mar del PlataMar del PlataArgentina
  3. 3.Grupo de Aprendizaje y Cognición Comparada, Laboratorio de Biología del Comportamiento, Instituto de Biología y Medicina Experimental (IBYME-CONICET), Facultad de PsicologíaUniversidad de Buenos AiresCiudad de Buenos AiresArgentina

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