Novelty at second glance: A critical appraisal of the novel-object paradigm based on meta-analysis

The study of consistent individual differences in behaviour has become an important focus in research on animal behaviour. Behavioural phenotypes are typically measured through standardized testing paradigms and one frequently used paradigm is the novel object test. In novel object tests, animals are exposed to new (unknown) objects and their reaction is quantified. When repeating trials to assess the temporal consistency of individual differences, researchers face the dilemma of whether to use the same or different ‘novel’ objects, since the same stimulus can result in habituation, while exposure to different objects can result in context-dependent responses. We performed a quantitative assessment of 254 effect sizes from 113 studies on novel-object trials to evaluate the properties of this testing paradigm, in particular the effect of object novelty and time interval between novel-object trials on estimates of individual consistency. We found an increase of sample sizes and an increase of estimates of repeatabilities with time. The vast majority of short-term studies (one month) used either the same or different novel objects about equally often. The average estimate for individual consistency was r = 0.47 (short-term r = 0.52, long-term r = 0.44). Novelty, time interval between trials and their interaction together explained only 3% of the total heterogeneity. Overall, novelobject trials reliably estimate individual differences in behaviour, but results were very heterogeneous even within the same study species, suggesting susceptibility to unknown details in testing conditions. Most studies that measure novel-object responses in association with food label the trait as neophobia, while novel-object trials in a neutral context are labelled variously as boldness/shyness, exploratory behaviour or neophobia/neophilia. Neophobia/neophilia is also the term most specific to novel object presentations. To avoid ambiguity, we suggest object neophobia/neophilia as the most specific label for novel-object responses.

[1]  M. I. Kaiser,et al.  What is an animal personality? , 2021, Biology & Philosophy.

[2]  J. Malmkvist,et al.  Development and consistency of fearfulness in horses from foal to adult , 2020 .

[3]  M. Ferkin,et al.  Long‐term repeatability and stability of three personality traits in meadow voles , 2020 .

[4]  A. M. Flanagan,et al.  Age-related patterns of neophobia in an endangered island crow: implications for conservation and natural history , 2020, Animal Behaviour.

[5]  Individual exploratory responses are not repeatable across time or context for four species of food-storing corvid , 2020, Scientific Reports.

[6]  S. Peters,et al.  Performance on tests of cognitive ability is not repeatable across years in a songbird , 2019, Animal Behaviour.

[7]  G. Kempermann,et al.  Early-life environmental enrichment generates persistent individualized behavior in mice , 2019, Science Advances.

[8]  A. Guenther,et al.  Validating standardised personality tests under semi‐natural conditions in wild house mice ( Mus musculus domesticus ) , 2019, Ethology.

[9]  R. Palme,et al.  Coping with style: individual differences in responses to environmental variation , 2019, Behavioral Ecology and Sociobiology.

[10]  O. Krüger,et al.  Intrinsic and maternal traits influence personality during early life in Galápagos sea lion, Zalophus wollebaeki, pups , 2019, Animal Behaviour.

[11]  S. Hatch,et al.  Boldness, mate choice and reproductive success in Rissa tridactyla , 2019, Animal Behaviour.

[12]  B. Doligez,et al.  No evidence for behavioural syndrome and genetic basis for three personality traits in a wild bird population , 2019, Animal Behaviour.

[13]  Kimberley J. Mathot,et al.  The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta‐analytic insights , 2018, Biological reviews of the Cambridge Philosophical Society.

[14]  M. Whiting,et al.  Can behaviour explain invasion success? A comparison between sympatric invasive and native lizards , 2019, Animal Behaviour.

[15]  H. Tan,et al.  Individual- and population-level personalities in a floriphilic katydid , 2019, Ethology.

[16]  K. Sewall,et al.  The effect of social context on measures of boldness: Zebra finches (Taeniopygia guttata) are bolder when housed individually , 2018, Behavioural Processes.

[17]  M. Hirata,et al.  Novel object response in beef cattle grazing a pasture as a group , 2018, Behavioural Processes.

[18]  Joel L. Pick,et al.  Reproducible, flexible and high‐throughput data extraction from primary literature: The metaDigitise r package , 2018, Methods in Ecology and Evolution.

[19]  R. Ha,et al.  Evidence for personality conformity, not social niche specialization in social jays , 2018 .

[20]  O. Krüger,et al.  Cortisol during adolescence organises personality traits and behavioural syndromes , 2018, Hormones and Behavior.

[21]  C. Gilbert,et al.  Development of an observational quantitative temperament test in three common parrot species , 2018 .

[22]  Courtney R. Garrison,et al.  Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis , 2018, Behavioral Ecology and Sociobiology.

[23]  Jessica Gurevitch,et al.  Meta-analysis and the science of research synthesis , 2018, Nature.

[24]  J. Eccard,et al.  The fast and the flexible: cognitive style drives individual variation in cognition in a small mammal , 2018, Animal Behaviour.

[25]  T. Burke,et al.  Extra-pair parentage and personality in a cooperatively breeding bird , 2018, Behavioral Ecology and Sociobiology.

[26]  João Pedro de Magalhães,et al.  Human Ageing Genomic Resources: new and updated databases , 2017, Nucleic Acids Res..

[27]  G. Leboucher,et al.  Personality traits and behavioural profiles in the domestic canary are affected by sex and photoperiod , 2017 .

[28]  T. Wright,et al.  Cognition, personality, and stress in budgerigars, Melopsittacus undulatus , 2017, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[29]  E. Wagenmakers,et al.  Detecting and avoiding likely false‐positive findings – a practical guide , 2017, Biological reviews of the Cambridge Philosophical Society.

[30]  K. Holekamp,et al.  Human disturbance affects personality development in a wild carnivore , 2017, Animal Behaviour.

[31]  L. Pedersen,et al.  Evaluating measures of exploratory behaviour in sows around farrowing and during lactation—A pilot study , 2017 .

[32]  A. Guenther,et al.  Individual consistency in multiple cognitive performance: behavioural versus cognitive syndromes , 2017, Animal Behaviour.

[33]  O. Leimar,et al.  A comparison of animal personality and coping styles in the red junglefowl , 2017, Animal Behaviour.

[34]  H. Schielzeth,et al.  Long-term effects of early nutrition and environmental matching on developmental and personality traits in zebra finches , 2017, Animal Behaviour.

[35]  N. Pillay,et al.  Active and explorative individuals are often restless and excluded from studies measuring resting metabolic rate: Do alternative metabolic rate measures offer a solution? , 2017, Physiology & Behavior.

[36]  D. Westneat,et al.  Foraging sparrows exhibit individual differences but not a syndrome when responding to multiple kinds of novelty , 2017 .

[37]  Malcolm F. Rosenthal,et al.  Taxonomic bias in animal behaviour publications , 2017, Animal Behaviour.

[38]  J. Gaillard,et al.  Neophobia is linked to behavioural and haematological indicators of stress in captive roe deer , 2017, Animal Behaviour.

[39]  R. N. Muzio,et al.  Neophobia is negatively related to reversal learning ability in females of a generalist bird of prey, the Chimango Caracara, Milvago chimango , 2017, Animal Cognition.

[40]  Yan-ping Huang,et al.  Do opposites attract? Effects of personality matching in breeding pairs of captive giant pandas on reproductive success , 2017 .

[41]  M. Lagisz,et al.  Metabolic rates, and not hormone levels, are a likely mediator of between-individual differences in behaviour: a meta-analysis , 2017 .

[42]  T. Burke,et al.  Repeatable and heritable behavioural variation in a wild cooperative breeder , 2017, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[43]  A. S. Griffin,et al.  Revisiting the open-field test: what does it really tell us about animal personality? , 2017, Animal Behaviour.

[44]  Françoise Lermite,et al.  Personality and problem-solving in common mynas (Acridotheres tristis) , 2017, Behavioural Processes.

[45]  D. Weary,et al.  Inconsistency in dairy calves’ responses to tests of fearfulness , 2016 .

[46]  Joseph W. Brown,et al.  rotl: an R package to interact with the Open Tree of Life data , 2016 .

[47]  Maxime Cauchoix,et al.  Personality does not predict social dominance in wild groups of black-capped chickadees , 2016, Animal Behaviour.

[48]  Heiko G. Rödel,et al.  Personality modulates proportions of CD4+ regulatory and effector T cells in response to socially induced stress in a rodent of wild origin , 2016, Physiology & Behavior.

[49]  N. Clayton,et al.  Seasonal changes in neophobia and its consistency in rooks: the effect of novelty type and dominance position , 2016, Animal Behaviour.

[50]  O. Burman,et al.  The impact of egg incubation temperature on the personality of oviparous reptiles , 2016, Animal Cognition.

[51]  T. Balsby,et al.  Personality matters: Consistency of inter-individual variation in shyness-boldness across non-breeding and pre-breeding season despite a fall in general shyness levels in farmed American mink (Neovison vison) , 2016 .

[52]  F. Suchentrunk,et al.  Shy is sometimes better: personality and juvenile body mass affect adult reproductive success in wild boars, Sus scrofa , 2016, Animal Behaviour.

[53]  N. Pillay,et al.  Personality traits are consistent when measured in the field and in the laboratory in African striped mice (Rhabdomys pumilio) , 2016, Behavioral Ecology and Sociobiology.

[54]  K. Herborn,et al.  Individual variation in corticosterone and personality traits in the blue tit Cyanistes caeruleus , 2016 .

[55]  F. Trillmich,et al.  Match–Mismatch Experiments Using Photoperiod Expose Developmental Plasticity of Personality Traits , 2016 .

[56]  N. Clayton,et al.  Neophobia is not only avoidance: improving neophobia tests by combining cognition and ecology , 2015, Current Opinion in Behavioral Sciences.

[57]  L. Garamszegi,et al.  Among-year variation in the repeatability, within- and between-individual, and phenotypic correlations of behaviors in a natural population , 2015, Behavioral Ecology and Sociobiology.

[58]  T. Balsby,et al.  Context Matters: Multiple Novelty Tests Reveal Different Aspects of Shyness-Boldness in Farmed American Mink (Neovison vison) , 2015, PloS one.

[59]  N. Pillay,et al.  Personality does not constrain social and behavioural flexibility in African striped mice , 2015, Behavioral Ecology and Sociobiology.

[60]  W. Shelledy,et al.  Genetic Influences on Response to Novel Objects and Dimensions of Personality in Papio Baboons , 2015, Behavior genetics.

[61]  A. Sih,et al.  The contribution of additive genetic variation to personality variation: heritability of personality , 2015, Proceedings of the Royal Society B: Biological Sciences.

[62]  J. G. Burleigh,et al.  Synthesis of phylogeny and taxonomy into a comprehensive tree of life , 2014, Proceedings of the National Academy of Sciences.

[63]  Gonçalo C. Cardoso,et al.  Social Dominance in a Gregarious Bird is Related to Body Size But not to Standard Personality Assays , 2015 .

[64]  Niels J Dingemanse,et al.  Animal personality and state-behaviour feedbacks: a review and guide for empiricists. , 2015, Trends in ecology & evolution.

[65]  Personality and density affect nest defence and nest survival in the great tit , 2015, acta ethologica.

[66]  J. Dupré The role of behaviour in the recurrence of biological processes , 2014 .

[67]  C. Mettke-Hofmann Article Type: Advanced Review Cognitive Ecology – Ecological Factors, Life-styles and Cognition , 2022 .

[68]  I. Krams,et al.  Sex‐Specific Associations Between Nest Defence, Exploration and Breathing Rate in Breeding Pied Flycatchers , 2014 .

[69]  C. Müller,et al.  Diet dependent experience and physiological state shape the behavior of a generalist herbivore , 2014, Physiology & Behavior.

[70]  F. Trillmich,et al.  The ontogeny of personality in the wild guinea pig , 2014, Animal Behaviour.

[71]  Culum Brown,et al.  Personality affects learning and trade-offs between private and social information in guppies, Poecilia reticulata , 2014, Animal Behaviour.

[72]  F. Trillmich,et al.  Learning and personality types are related in cavies (Cavia aperea). , 2014, Journal of comparative psychology.

[73]  T. L. Dzieweczynski,et al.  The effects of 17α-ethinyloestradiol on boldness and its relationship to decision making in male Siamese fighting fish , 2014, Animal Behaviour.

[74]  J. Grace,et al.  Personality correlates with contextual plasticity in a free-living, long-lived seabird , 2014 .

[75]  A. Angerbjörn,et al.  Situation and context impacts the expression of personality: The influence of breeding season and test context , 2013, Behavioural Processes.

[76]  A. Mutzel,et al.  Slow explorers take less risk: a problem of sampling bias in ecological studies , 2013 .

[77]  H. Schielzeth,et al.  Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity? , 2013, Global change biology.

[78]  N. Clayton,et al.  Dominance, pair bonds and boldness determine social-foraging tactics in rooks, Corvus frugilegus , 2013, Animal Behaviour.

[79]  A. J. Frost,et al.  Environmental change alters personality in the rainbow trout, Oncorhynchus mykiss , 2013, Animal Behaviour.

[80]  P. Poncin,et al.  Neophobia and social tolerance are related to breeding group size in a semi-colonial bird , 2013, Behavioral Ecology and Sociobiology.

[81]  G. Cowlishaw,et al.  Animal personality: what are behavioural ecologists measuring? , 2013, Biological reviews of the Cambridge Philosophical Society.

[82]  F. Trillmich,et al.  Photoperiod influences the behavioral and physiological phenotype during ontogeny , 2013 .

[83]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[84]  Kerrie Mengersen,et al.  Handbook of Meta-analysis in Ecology and Evolution , 2013 .

[85]  D. Westneat,et al.  Individual and Sex Differences in Habituation and Neophobia in House Sparrows (Passer domesticus) , 2012 .

[86]  Melanie Dammhahn,et al.  Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness , 2012, Animal Behaviour.

[87]  C. Mettke-Hofmann,et al.  Head Colour and Age Relate to Personality Traits in Gouldian Finches , 2012 .

[88]  J. Cassady,et al.  Relationship between backtest and coping styles in pigs , 2012 .

[89]  Franz J Weissing,et al.  Animal personalities: consequences for ecology and evolution. , 2012, Trends in ecology & evolution.

[90]  J. Grindstaff,et al.  Maternal and developmental immune challenges alter behavior and learning ability of offspring , 2012, Hormones and Behavior.

[91]  Z. Barta,et al.  Personality traits across ontogeny in firebugs, Pyrrhocoris apterus , 2012, Animal Behaviour.

[92]  C. Mettke-Hofmann,et al.  Colourful characters: head colour reflects personality in a social bird, the Gouldian finch, Erythrura gouldiae , 2012, Animal Behaviour.

[93]  M. Eens,et al.  Corticosterone, Avoidance of Novelty, Risk-Taking and Aggression in a Wild Bird: No Evidence for Pleiotropic Effects , 2012 .

[94]  Christina Rockwell,et al.  Bolder, older, and selective: factors of individual-specific foraging behaviors in Steller’s jays , 2012 .

[95]  Å. Krogdahl,et al.  Context-dependent responses to novelty in Rainbow trout (Oncorhynchus mykiss), selected for high and low post-stress cortisol responsiveness , 2012, Physiology & Behavior.

[96]  Shinichi Nakagawa,et al.  Methodological issues and advances in biological meta-analysis , 2012, Evolutionary Ecology.

[97]  A. S. Griffin,et al.  Consumer and motor innovation in the common myna: the role of motivation and emotional responses , 2012, Animal Behaviour.

[98]  S. MacDougall-Shackleton,et al.  Song bout length is indicative of spatial learning in European starlings , 2012 .

[99]  S. Wieren,et al.  No evidence for negative frequency–dependent feeding performance in relation to personality , 2012 .

[100]  M. Taborsky,et al.  Individual variation in helping in a cooperative breeder: relatedness versus behavioural type , 2011, Animal Behaviour.

[101]  M. David,et al.  Personality predicts social dominance in female zebra finches, Taeniopygia guttata, in a feeding context , 2011, Animal Behaviour.

[102]  B. Kempenaers,et al.  Quantitative genetics and fitness consequences of neophilia in zebra finches , 2011 .

[103]  Shinichi Nakagawa,et al.  Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists , 2010, Biological reviews of the Cambridge Philosophical Society.

[104]  Wolfgang Viechtbauer,et al.  Conducting Meta-Analyses in R with the metafor Package , 2010 .

[105]  Robert B. Gramacy,et al.  amei: An R Package for the Adaptive Management of Epidemiological Interventions , 2010 .

[106]  K. Herborn,et al.  Personality in captivity reflects personality in the wild , 2010, Animal Behaviour.

[107]  T. Laaksonen,et al.  Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca) , 2010, Hormones and Behavior.

[108]  K. Oers,et al.  Personality differences explain leadership in barnacle geese , 2009, Animal Behaviour.

[109]  Kate L. Laskowski,et al.  The repeatability of behaviour: a meta-analysis , 2009, Animal Behaviour.

[110]  Pablo Michelena,et al.  Effects of group size and personality on social foraging: the distribution of sheep across patches , 2009 .

[111]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2009, Journal of clinical epidemiology.

[112]  C. Ioannou,et al.  Ecological consequences of the bold–shy continuum: the effect of predator boldness on prey risk , 2008, Oecologia.

[113]  Daniel T. Blumstein,et al.  Fitness consequences of personality: a meta-analysis , 2008 .

[114]  M. Tobler,et al.  Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata , 2007, Hormones and Behavior.

[115]  N. Dingemanse,et al.  Integrating animal temperament within ecology and evolution , 2007, Biological reviews of the Cambridge Philosophical Society.

[116]  Kevin N. Laland,et al.  The relation between social rank, neophobia and individual learning in starlings , 2006, Animal Behaviour.

[117]  J. Garner,et al.  Is fearfulness a trait that can be measured with behavioural tests? A validation of four fear tests for Japanese quail , 2006, Animal Behaviour.

[118]  John P. A. Ioannidis,et al.  Assessing the Evolution of Effect Sizes over Time , 2006 .

[119]  P. Drent,et al.  Personalities in great tits, Parus major: stability and consistency , 2005, Animal Behaviour.

[120]  Alexander D. M. Wilson,et al.  Consistency in Context-specific Measures of Shyness and Boldness in Rainbow Trout, Oncorhynchus mykiss , 2005 .

[121]  J. Garner,et al.  The test–retest reliability of four behavioural tests of fearfulness for quail: a critical evaluation , 2005 .

[122]  M. Eens,et al.  Unravelling animal personalities: how and why individuals consistently differ , 2005 .

[123]  Sara M. Stieb,et al.  Personality traits in resident and migratory warbler species. , 2005 .

[124]  N. Dingemanse,et al.  Natural selection and animal personality , 2005 .

[125]  A. Sih,et al.  Behavioral Syndromes: An Integrative Overview , 2004, The Quarterly Review of Biology.

[126]  L. Pedersen,et al.  Aggression, fearfulness and coping styles in female pigs , 2003 .

[127]  J. Mench,et al.  Environmental enrichment affects the fear and exploratory responses to novelty of young Amazon parrots , 2002 .

[128]  J. Malmkvist,et al.  Generalization of fear in farm mink, Mustela vison, genetically selected for behaviour towards humans , 2002, Animal Behaviour.

[129]  D. Roff,et al.  Selection, structure and the heritability of behaviour , 2002 .

[130]  H. Winkler,et al.  The significance of ecological factors for exploration and neophobia in parrots , 2002 .

[131]  P. Levin,et al.  Integrating individual behavior and population ecology: the potential for habitat-dependent population regulation in a reef fish , 2000 .

[132]  G. Smith,et al.  Bias in meta-analysis detected by a simple, graphical test , 1997, BMJ.

[133]  V. Pedersen Long-term effects of different handling procedures on behavioural, physiological, and production-related parameters in silver foxes , 1994 .

[134]  W. Hopkins,et al.  Handedness and approach-avoidance behavior in chimpanzees (Pan). , 1994, Journal of experimental psychology. Animal behavior processes.

[135]  J. M. Smith,et al.  Optimality theory in evolutionary biology , 1990, Nature.

[136]  R. Greenberg Feeding neophobia and ecological plasticity: a test of the hypothesis with captive sparrows , 1990, Animal Behaviour.

[137]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[138]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[139]  D. Berlyne Curiosity and exploration. , 1966, Science.

[140]  R. Yerkes,et al.  Nature and conditions of avoidance (fear) response in chimpanzee. , 1936 .