Abstract
Aquatic habitats are extremely dynamic, with constantly changing ecological factors, which has now been exacerbated due to human-induced rapid environmental change. In such variable environments, it becomes essential to understand how personality and cognition in organisms affect the adaptability of individuals to different habitat conditions. To test this, we studied how personality-related traits as well as cognitive ability differ between populations of wild-caught zebrafish (Danio rerio) from habitats that differed in various environmental factors. We measured emergence into a novel environment as an indicator of boldness, and performance in a spatial task inferred from feeding latencies in a maze over repeated trials to assess learning and memory, as an indicator of cognitive ability. We found that personality affects cognition and although bolder fish are better learners, they show poorer retention of memory across populations. Although personality and cognitive ability varied between habitats, the patterns of their correlations remained similar within each population. However, the individual traits (such as sex and size) that were drivers of personality and cognition differed between the habitats, suggesting that not only do behavioral traits vary between populations, but also the factors that are important in determining them. Personality and cognitive ability and the correlations between these traits determine how well an organism performs in its habitat, as well as how likely it is to find new habitats and adapt to them. Studying these across wild zebrafish populations helps predict performance efficiencies among individuals and also explains how fish adapt to extremely dynamic environments that can lead to variation in behavioral traits and correlations between them. This study not only sheds light on the drivers of interindividual variation and co-occurrence patterns of personality and cognition, but also individual and population factors that might have an effect on them.
Similar content being viewed by others
Data availability
Data obtained from observations will be made available by the authors on request to the corresponding author.
References
Arunachalam M, Raja M, Vijayakumar C, Malaiammal P, Mayden RL (2013) Natural history of zebrafish (Danio rerio) in India. Zebrafish 10(1):1–14
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Bengston SE, Dornhaus A (2014) Be meek or be bold? a colony-level behavioural syndrome in ants. Proceed Royal Soc B Biol Sci 281(1791):20140518
Bhat A, Greulich MM, Martins EP (2015) Behavioral plasticity in response to environmental manipulation among zebrafish (Danio rerio) populations. PLoS ONE 10(4):e0125097
Bókony V, Kulcsár A, Tóth Z, Liker A (2012) Personality traits and behavioral syndromes in differently urbanized populations of house sparrows (Passer domesticus). PLoS ONE 7(5):e36639
Brashares JS, Arcese P (2002) Role of forage, habitat and predation in the behavioural plasticity of a small African antelope. J Anim Ecol 71:626–638
Briffa M, Weiss A (2010) Animal personality. Curr Biol 20(21):R912–R914
Brust V, Guenther A (2017) Stability of the guinea pigs personality–cognition–linkage over time. Behav Proc 134:4–11
Carbia PS, Brown C (2019) Environmental enrichment influences spatial learning ability in captive-reared intertidal gobies (Bathygobius cocosensis). Anim Cogn 22(1):89–98
Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57(4):491–498
Colléter M, Brown C (2011) Personality traits predict hierarchy rank in male rainbowfish social groups. Anim Behav 81(6):1231–1237
Dadda M, Domenichini A, Piffer L, Argenton F, Bisazza A (2010) Early differences in epithalamic left–right asymmetry influence lateralization and personality of adult zebrafish. Behav Brain Res 206(2):208–215
Dall SR, Griffith SC (2014) An empiricist guide to animal personality variation in ecology and evolution. Front Ecol Evol 2:3
Daniel DK, Bhat A (2020) Bolder and Brighter? Exploring correlations between personality and cognitive abilities among individuals within a population of wild zebrafish Danio Rerio. Front Behav Neurosci 14:138
Daniel DK, Bhat A (2022) Sex and population drive interindividual variations in a cognitive task across three populations of wild zebrafish. Front Psychol. https://doi.org/10.3389/fpsyg.2022.786486
Del Giudice M (2012) Sex ratio dynamics and fluctuating selection on personality. J Theor Biol 297:48–60
Delignette-Muller ML, Dutang C (2015) fitdistrplus: An R package for fitting distributions. J Stat Softw 64(4):1–34
DePasquale C, Fettrow S, Sturgill J, Braithwaite VA (2019) The impact of flow and physical enrichment onpreferences in zebrafish. Appl Ani Behav Sci 215:77–81
Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184
Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76(6):1128–1138
Dosmann A, Mateo JM (2014) Food, sex and predators: animal personality persists with multidimensional plasticity across complex environments. Anim Behav 90:109–116
Dougherty LR, Guillette LM (2018) Linking personality and cognition: a meta-analysis. Phil Trans R Soc B Biol Sci 373(1756):20170282
Downes SJ, Adams M (2001) Geographic variation in antisnake tactics: the evolution of scent-mediated behavior in a lizard. Evolution 55(3):605–615
Dubuc-Messier G, Réale D, Perret P, Charmantier A (2017) Environmental heterogeneity and population differences in blue tits personality traits. Behav Ecol 28(2):448–459
Eggers DM (1982) Planktivore preference by prey size. Ecology 63(2):381–390
Engeszer RE, Patterson LB, Rao AA, Parichy DM (2007) Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4(1):21–40
Evans J, Boudreau K, Hyman J (2010) Behavioural syndromes in urban and rural populations of song sparrows. Ethology 116(7):588–595
Foster SA (1995) Understanding the evolution of behavior in threespine stickleback: the value of geographic variation. Behaviour 132(15–16):1107–1129
Garnham L, Løvlie H (2018) Sophisticated fowl: the complex behaviour and cognitive skills of chickens and red junglefowl. Behav Sci 8(1):13
Garnham LC, Porthén SA, Child S, Forslind S, Løvlie H (2019) The role of personality, cognition, and affective state in same-sex contests in the red junglefowl. Behav Ecol Sociobiol 73(11):1–12
Gill AB, Hart PJ (1994) Feeding behaviour and prey choice of the threespine stickleback: the interacting effects of prey size, fish size and stomach fullness. Anim Behav 47(4):921–932
Griffin AS, Guillette LM, Healy SD (2015) Cognition and personality: an analysis of an emerging field. Trends Ecol Evol 30(4):207–214
Guenther A, Brust V, Dersen M, Trillmich F (2014) Learning and personality types are related in cavies (Cavia aperea). J Comp Psychol 128(1):74
Guillette LM, Naguib M, Griffin AS (2017) Individual differences in cognition and personality. Behav Process 134:1–3
Hannunen S, Ekbom B (2002) Within species variation in host plant quality and movement behavior of Lygus rugulipennis nymphs. Entomol Exp Appl 104(1):95–101
Head ML, Lindholm AK, Brooks R (2008) Operational sex ratio and density do not affect directional selection on male sexual ornaments and behavior. Evol Int J Org Evol 62(1):135–144
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(4):835–847
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363
Hutchings JA, Morris DW (1985) The influence of phylogeny, size and behaviour on patterns of covariation in salmonid life histories. Oikos 45:118–124
Irving E, Brown C (2013) Examining the link between personality and laterality in a feral guppy Poecilia reticulata population. J Fish Biol 83(2):311–325
Jayakody S, Sibbald AM, Gordon IJ, Lambin X (2008) Red deer Cervus elephus vigilance behaviour differs with habitat and type of human disturbance. Wildl Biol 14(1):81–91
Jenouvrier S, Caswell H, Barbraud C, Weimerskirch H (2010) Mating behavior, population growth, and the operational sex ratio: a periodic two-sex model approach. Am Nat 175(6):739–752
Kareklas K, Elwood RW, Holland RA (2017) Personality effects on spatial learning: comparisons between visual conditions in a weakly electric fish. Ethology 123(8):551–559
Kelly JR, Shelton SG, Daniel DK, Bhat A, Mondal R, Nipple F, Shelton DS (2021) Wild zebrafish sentinels: biological monitoring of site differences using behavior and morphology. Toxics 9(7):165
Ketterson ED (1979) Aggressive behavior in wintering dark-eyed juncos: determinants of dominance and their possible relation to geographic variation in sex ratio. Wilson Bull 91:371–383
King JE (2007) Dimensions of the ape mind: adding personality to behavior and cognition. In: Washburn DA (ed) Primate perspectives on behavior and cognition. American Psychological Association, pp 47–60
Kralj-Fišer S, Hebets EA, Kuntner M (2017) Different patterns of behavioral variation across and within species of spiders with differing degrees of urbanization. Behav Ecol Sociobiol 71(8):1–15
Kroodsma DE, Byers BE, Halkin SL, Hill C, Minis D, Bolsinger JR, Wilda K (1999) Geographic variation in black-capped chickadee songs and singing behavior. Auk 116(2):387–402
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26
Liu M, Liu Y, Wang H, Jia J, Liu K (2022) Color discrimination provides insight into the relationship between personality cognition and brain morphology in the western mosquitofish (Gambusia affinis). Brain Behav Evol 97:274–283
Locurto C (2007) Individual differences and animal personality. Comparat Cogn Behav Rev 2(1):67–78
Lucon-Xiccato T, Dadda M (2017) Personality and cognition: sociability negatively predicts shoal size discrimination performance in guppies. Front Psychol 8:1118
Lucon-Xiccato T, Montalbano G, Bertolucci C (2020a) Personality traits covary with individual differences in inhibitory abilities in 2 species of fish. Curr Zool 66(2):187–195
Lucon-Xiccato T, Montalbano G, Dadda M, Bertolucci C (2020b) Lateralization correlates with individual differences in inhibitory control in zebrafish. Biol Let 16(8):20200296
Magurran AE (1999) The causes and consequences of geographic variation in antipredator behavior: perspectives from fish populations. In: Margurran AE (ed) Geographic variation in behavior. Oxford University Press, UK
Martins EP, Bhat A (2014) Population-level personalities in zebrafish: aggression-boldness across but not within populations. Behav Ecol 25(2):368–373
Mayer M, Shine R, Brown GP (2016) Bigger babies are bolder: effects of body size on personality of hatchling snakes. Behaviour 153(3):313–323
Medina-García A, Jawor JM, Wright TF (2017) Cognition, personality, and stress in budgerigars Melopsittacus Undulatus. Behav Ecol 28(6):1504–1516
Michelangeli M, Cote J, Chapple DG, Sih A, Brodin T, Fogarty S, Wong BB (2020) Sex-dependent personality in two invasive species of mosquitofish. Biol Invasions 22(4):1353–1364
Miletto Petrazzini ME, Pecunioso A, Dadda M, Agrillo C (2019) the impact of brain lateralization and anxiety-like behaviour in an extensive operant conditioning task in zebrafish (Danio rerio). Symmetry 11(11):1395
Moura RR, Peixoto PEC (2013) The effect of operational sex ratio on the opportunity for sexual selection: a meta-analysis. Anim Behav 86(4):675–683
Naguib M, Flörcke C, van Oers K (2011) Effects of social conditions during early development on stress response and personality traits in great tits (Parus major). Dev Psychobiol 53(6):592–600
Niemelä PT, Vainikka A, Forsman JT, Loukola OJ, Kortet R (2013) How does variation in the environment and individual cognition explain the existence of consistent behavioral differences? Ecol Evol 3(2):457–464
Parichy DM (2015) The natural history of model organisms: Advancing biology through a deeper understanding of zebrafish ecology and evolution. Elife 4:e05635
Parkos JJ III, Wahl DH (2010) Influence of body size and prey type on the willingness of age-0 fish to forage under predation risk. Trans Am Fish Soc 139(4):969–975
Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Roy T, Bhat A (2016) Learning and memory in juvenile zebrafish: what makes the difference–population or rearing environment? Ethology 122(4):308–318
Roy T, Bhat A (2017) Social learning in a maze? contrasting individual performance among wild zebrafish when associated with trained and naïve conspecifics. Behav Proc 144:51–57
Roy T, Bhat A (2018a) Repeatability in boldness and aggression among wild zebrafish (Danio rerio) from two differing predation and flow regimes. J Comp Psychol 132(4):349
Roy T, Bhat A (2018b) Population, sex and body size: determinants of behavioural variations and behavioural correlations among wild zebrafish Danio rerio. R Soc Open Sci 5(1):170978
Roy T, Shukla R, Bhat A (2017) Risk-taking during feeding: between-and within-population variation and repeatability across contexts among wild zebrafish. Zebrafish 14(5):393–403
Savaşçı BB, Lucon-Xiccato T, Bisazza A (2021) Ontogeny and personality affect inhibitory control in guppies, Poecilia reticulata. Anim Behav 180:111–121
Schuett W, Dall SR (2009) Sex differences, social context and personality in zebra finches Taeniopygia Guttata. Anim Behav 77(5):1041–1050
Seghers BH (1974) Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia 14(1):93–98
Shelton DS, Shelton SG, Daniel DK, Raja M, Bhat A, Tanguay RL, Martins EP (2020) Collective behavior in wild zebrafish. Zebrafish 17(4):243–252
Shukla R, Bhat A (2017) Morphological divergences and ecological correlates among wild populations of zebrafish (Danio rerio). Environ Biol Fishes 100(3):251–264
Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish. Danio Rerio Biol Rev 83(1):13–34
Spence R, Magurran AE, Smith C (2011) Spatial cognition in zebrafish: the role of strain and rearing environment. Anim Cogn 14(4):607–612
Stamps J, Groothuis TG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85(2):301–325
Stearns SC (1989) The evolutionary significance of phenotypic plasticity. Bioscience 7:436–445
Streit RP, Bellwood DR (2017) High prevalence of homing behaviour among juvenile coral-reef fishes and the role of body size. Coral Reefs 36(4):1083–1095
Suriyampola PS, Shelton DS, Shukla R, Roy T, Bhat A, Martins EP (2016) Zebrafish social behavior in the wild. Zebrafish 13(1):1–8
Wallace KJ, Rausch RT, Ramsey ME, Cummings ME (2020) Sex differences in cognitive performance and style across domains in mosquitofish (Gambusia affinis). Anim Cogn 23(4):655–669
Weiss A (2018) Personality traits: a view from the animal kingdom. J Pers 86(1):12–22
White SL, Wagner T, Gowan C, Braithwaite VA (2017) Can personality predict individual differences in brook trout spatial learning ability? Behav Proc 141:220–228
Whiteley AR, Bhat A, Martins EP, Mayden RL, Arunachalam M, Uusi-Heinkkilä SILVA, Bernatchez L (2011) Population genomics of wild and laboratory zebrafish (Danio rerio). Mol Ecol 20(20):4259–4276
Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York
Wright D, Rimmer LB, Pritchard VL, Butlin RK, Krause J (2003) Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). J Fish Biol 63:258–259
Zidar J, Sorato E, Malmqvist AM, Jansson E, Rosher C, Jensen P, Løvlie H (2017) Early experience affects adult personality in the red junglefowl: a role for cognitive stimulation? Behav Process 134:78–86
Zidar J, Balogh A, Favati A, Jensen P, Leimar O, Sorato E, Løvlie H (2018) The relationship between learning speed and personality is age-and task-dependent in red junglefowl. Behav Ecol Sociobiol 72(10):1–13
Acknowledgements
The authors would like to thank the Indian Institute of Science Education and Research Kolkata, (IISER Kolkata), India for providing infrastructural support, and Council for Science and Industrial Research (CSIR), Government of India, for providing a Senior Research Fellowship to DKD. Authors also thank Mr. Prasenjit Pan for collection of wild zebrafish populations from different habitats, and all members of the Fish Ecology and Behaviour Lab, IISER Kolkata, for lab and population maintenance.
Funding
AB received institutional financial support in the form of Academic Research Funds from Indian Institute of Science Kolkata (India). DKD was funded through a junior and senior research fellowship from the Council of Science and Industrial Research (CSIR), Government of India.
Author information
Authors and Affiliations
Contributions
DKD and AB conceived the goals and the design of the study. DKD conducted the experimental assays, analyzed the videos, performed the statistical analyses and wrote the first draft of the manuscript. AB procured funding and supervised the project. DKD and AB wrote and edited the final version of manuscript. All authors read and approved the submitted version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Ethical approval
Guidelines outlined by the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA), Ministry of Fisheries, Animal Husbandry and Dairying, Government of India were followed in all aspects of maintenance and experimentation. All experimental protocols followed here have been approved by the Institutional Animal Ethics Committee's (IAEC) and guidelines of Indian Institute of Science Education and Research (IISER) Kolkata, Government of India (Approval number IISERK/IAEC/AP/2021/70).
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
Daniel, D.K., Bhat, A. Correlations begin at home: drivers of co-occurrence patterns in personality and cognitive ability in wild populations of zebrafish. Anim Cogn 26, 1381–1394 (2023). https://doi.org/10.1007/s10071-023-01787-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-023-01787-w