Laterality enhances numerical skills in the guppy, Poecilia reticulata

It has been hypothesized that cerebral lateralization can significantly enhance cognition and that this was one of the primary selective forces shaping its wide-spread evolution amongst vertebrate taxa. Here, we tested this hypothesis by examining the link between cerebral lateralization and numerical discrimination. Guppies, Poecilia reticulata, were sorted into left, right and non-lateralized groups using a standard mirror test and their numerical discrimination abilities tested in both natural shoal choice and abstract contexts. Our results show that strongly lateralized guppies have enhanced numerical abilities compared to non-lateralized guppies irrespective of context. These data provide further credence to the notion that cerebral lateralization can enhance cognitive efficiency.

[1]  Christian Agrillo,et al.  Numerical acuity of fish is improved in the presence of moving targets, but only in the subitizing range , 2013, Animal Cognition.

[2]  R. Gerlai,et al.  Spontaneous discrimination of small quantities: shoaling preferences in angelfish (Pterophyllum scalare) , 2011, Animal Cognition.

[3]  A. Giljov,et al.  Eye as a key element of conspecific image eliciting lateralized response in fish , 2013, Animal Cognition.

[4]  Claudia Uller,et al.  Quantity discrimination in salamanders , 2010, Journal of Experimental Biology.

[5]  M. Dadda,et al.  Does brain asymmetry allow efficient performance of simultaneous tasks? , 2006, Animal Behaviour.

[6]  G. Vallortigara,et al.  Laterality in detour behaviour: interspecific variation in poeciliid fish , 1997, Animal Behaviour.

[7]  L. Regolin,et al.  Advantages of a Lateralised Brain for Reasoning About the Social World in Chicks , 2013 .

[8]  P. Walmsley,et al.  Statistical Method , 1923, Nature.

[9]  Marco Dadda,et al.  Development and application of a new method to investigate cognition in newborn guppies , 2012, Behavioural Brain Research.

[10]  Susan Carey,et al.  Spontaneous number representation in semi–free–ranging rhesus monkeys , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  Jens Krause,et al.  Shoal choice in zebrafish, Danio rerio: the influence of shoal size and activity , 2001, Animal Behaviour.

[12]  C. Packer,et al.  Roaring and numerical assessment in contests between groups of female lions, Panthera leo , 1994, Animal Behaviour.

[13]  Elizabeth M Brannon,et al.  Basic Math in Monkeys and College Students , 2007, PLoS biology.

[14]  M. Beran.  Summation and numerousness judgments of sequentially presented sets of items by chimpanzees (Pan troglodytes). , 2001, Journal of comparative psychology.

[15]  Culum Brown,et al.  Laterality enhances cognition in Australian parrots , 2009, Proceedings of the Royal Society B: Biological Sciences.

[16]  Margot J. Taylor,et al.  Is 2+2=4? Meta-analyses of brain areas needed for numbers and calculations , 2011, NeuroImage.

[17]  A. Bisazza,et al.  Large Number Discrimination by Mosquitofish , 2010, PloS one.

[18]  Stanislas Dehaene,et al.  PSYCHOLOGICAL SCIENCE Research Article Does Subitizing Reflect Numerical Estimation? , 2022 .

[19]  E. Spelke,et al.  Language and Conceptual Development series Core systems of number , 2004 .

[20]  G. Rosenthal,et al.  Shoaling decisions in female swordtails: how do fish gauge group size? , 2007 .

[21]  Culum Brown,et al.  The Evolution of lateralized foot use in parrots : a phylogenetic approach , 2011 .

[22]  V. Nepomnyashchikh,et al.  Individual-level consistency of different laterality measures in the goldbelly topminnow. , 2012, Behavioral neuroscience.

[23]  A. Bisazza,et al.  Extensive training extends numerical abilities of guppies , 2014, Animal Cognition.

[24]  Bahador Bahrami,et al.  Collective enhancement of numerical acuity by meritocratic leadership in fish , 2014, Scientific reports.

[25]  D. Chivers,et al.  Brook Char (Salvelinus fontinalis) Can Differentiate Chemical Alarm Cues Produced by Different Age/Size Classes of Conspecifics , 2002, Journal of Chemical Ecology.

[26]  C. Agrillo,et al.  Turning to the larger shoal: are there individual differences in small- and large-quantity discrimination of guppies? , 2015 .

[27]  Russell D. Fernald,et al.  What do fish make of mirror images? , 2010, Biology Letters.

[28]  O. Güntürkün,et al.  Left hemispheric advantage for numerical abilities in the bottlenose dolphin , 2005, Behavioural Processes.

[29]  L. Rogers.  Lateralization in vertebrates: Its early evolution, general pattern, and development , 2002 .

[30]  L. A. Carneiro,et al.  Behavioural endocrinology: No hormonal response in tied fights , 2005, Nature.

[31]  G. Vallortigara,et al.  Mosquitofish display differential left- and right-eye use during mirror image scrutiny and predator inspection responses , 2001, Animal Behaviour.

[32]  Balázs Szentes,et al.  Spontaneous Discrimination , 2012 .

[33]  K. Burns,et al.  Adaptive numerical competency in a food-hoarding songbird , 2008, Proceedings of the Royal Society B: Biological Sciences.

[34]  L. Piffer,et al.  Large Number Discrimination in Newborn Fish , 2013, PloS one.

[35]  G. Vallortigara,et al.  Discrimination of small quantities by fish (redtail splitfin, Xenotoca eiseni) , 2013, Animal Cognition.

[36]  G. Vallortigara,et al.  Advantages of having a lateralized brain , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  Marco Dadda,et al.  Do fish count? Spontaneous discrimination of quantity in female mosquitofish , 2008, Animal Cognition.

[38]  R. Gerlai,et al.  Can angelfish (Pterophyllum scalare) count? Discrimination between different shoal sizes follows Weber’s law , 2010, Animal Cognition.

[39]  Joachim G. Frommen,et al.  Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish , 2014, Behavioral Ecology and Sociobiology.

[40]  G. W. Snedecor.  Statistical Methods , 1964 .

[41]  O. Güntürkün,et al.  Asymmetry pays: visual lateralization improves discrimination success in pigeons , 2000, Current Biology.

[42]  V. Braithwaite,et al.  Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi , 2005 .

[43]  Daniel C. Hyde,et al.  Small and large number discrimination in guppies , 2011, Animal Cognition.

[44]  M. Dadda,et al.  Emotional responsiveness in fish from lines artificially selected for a high or low degree of laterality , 2007, Physiology & Behavior.

[45]  Z. Reznikova,et al.  Quantity judgments in the context of risk/reward decision making in striped field mice: first “count,” then hunt , 2013, Front. Psychology.

[46]  B. Smuts,et al.  Quantity-based judgments in the domestic dog (Canis lupus familiaris) , 2006, Animal Cognition.

[47]  Marco Dadda,et al.  The costs of hemispheric specialization in a fish , 2009, Proceedings of the Royal Society B: Biological Sciences.

[48]  Wolfgang Grodd,et al.  Comparison of quantities: core and format-dependent regions as revealed by fMRI. , 2012, Cerebral cortex.

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

[50]  Justin Halberda,et al.  Individual differences in non-verbal number acuity correlate with maths achievement , 2008, Nature.

[51]  Brian Butterworth,et al.  Evidence for Two Numerical Systems That Are Similar in Humans and Guppies , 2012, PloS one.

[52]  Sarah Benson-Amram,et al.  Numerical assessment and individual call discrimination by wild spotted hyaenas, Crocuta crocuta , 2011, Animal Behaviour.

[53]  M. Beran.  Monkeys (Macaca mulatta and Cebus apella) track, enumerate, and compare multiple sets of moving items. , 2008, Journal of experimental psychology. Animal behavior processes.

[54]  P. E. Pisa,et al.  Quantity discrimination in felines: a preliminary investigation of the domestic cat (Felis silvestris catus) , 2009, Journal of Ethology.

[55]  Michael J. Beran,et al.  Quantity Perception by Adult Humans (Homo sapiens), Chimpanzees (Pan troglodytes), and Rhesus Macaques (Macaca mulatta) as a Function of Stimulus Organization , 2006, International Journal of Comparative Psychology.