Inter-Specific Differences in Numerical Abilities Among Teleost Fish

Adults, infants and non-human primates are thought to possess similar non-verbal numerical systems, but there is considerable debate regarding whether all vertebrates share the same numerical abilities. Despite an abundance of studies, cross-species comparison remains difficult because the methodology employed and the context of species examination vary considerably across studies. To fill this gap, we used the same procedure, stimuli, and numerical contrasts to compare quantity abilities of five teleost fish: redtail splitfin, guppies, zebrafish, Siamese fighting fish, and angelfish. Subjects were trained to discriminate between two sets of geometrical figures using a food reward. Fish initially were trained on an easy numerical ratio (5 vs. 10 and 6 vs. 12). Once they reached the learning criterion, they were subjected to non-reinforced probe trials in which the set size was constant but numerical ratios varied (8 vs. 12 and 9 vs. 12). They also were subjected to probe trials in which the ratio was constant, but the total set size was increased (25 vs. 50) or decreased (2 vs. 4). Overall, fish generalized to numerosities with a 0.67 ratio, but failed with a 0.75 ratio; they generalized to a smaller set size, but not to a larger one. Only minor differences were observed among the five species. However, in one species, zebrafish, the proportion of individuals reaching the learning criterion was much smaller than in the others. In a control experiment, zebrafish showed a similar lower performance in shape discrimination, suggesting that the observed difference resulted from the zebrafish’s difficulty in learning this procedure rather than from a cross-species variation in the numerical domain.

[1]  Boris Ryabko,et al.  Numerical competence in animals, with an insight from ants , 2011 .

[2]  Elizabeth S. Spelke,et al.  Evolutionary and developmental foundations of human knowledge: A case study of mathematics , 2004 .

[3]  S. Carey,et al.  The Representations Underlying Infants' Choice of More: Object Files Versus Analog Magnitudes , 2002, Psychological science.

[4]  R. J. Young,et al.  Do domestic dogs show any evidence of being able to count? , 2002, Animal Cognition.

[5]  M. Beran,et al.  Putting the elephant back in the herd: elephant relative quantity judgments match those of other species , 2012, Animal Cognition.

[6]  R. Jaeger,et al.  Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian , 2003, Animal Cognition.

[7]  Marco Dadda,et al.  Use of Number by Fish , 2009, PloS one.

[8]  M. Beran,et al.  Bears ‘count’ too: quantity estimation and comparison in black bears, Ursus americanus , 2012, Animal Behaviour.

[9]  T. Sato,et al.  Relative quantity judgment by Asian elephants (Elephas maximus) , 2008, Animal Cognition.

[10]  A. Fine,et al.  Olfactory conditioning in the zebrafish (Danio rerio) , 2009, Behavioural Brain Research.

[11]  Masaki Tomonaga,et al.  Enumeration of briefly presented items by the chimpanzee (Pan troglodytes) and humans (Homo sapiens) , 2002, Animal learning & behavior.

[12]  Onur Güntürkün,et al.  A bottlenose dolphin discriminates visual stimuli differing in numerosity , 2003, Learning & behavior.

[13]  A. Bisazza,et al.  Ontogeny of Numerical Abilities in Fish , 2010, PloS one.

[14]  J. Call,et al.  Discrete quantity judgments in the great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus): the effect of presenting whole sets versus item-by-item. , 2007, Journal of comparative psychology.

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

[16]  E. Brannon,et al.  The difficulties of representing continuous extent in infancy: using number is just easier. , 2008, Child development.

[17]  E. Font,et al.  Quantity discrimination in Tenebrio molitor: evidence of numerosity discrimination in an invertebrate? , 2008, Animal Cognition.

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

[19]  N. Giret,et al.  The discrimination of discrete and continuous amounts in African grey parrots (Psittacus erithacus) , 2008, Animal Cognition.

[20]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[21]  Peter Dixon,et al.  Likelihood ratios: A simple and flexible statistic for empirical psychologists , 2004, Psychonomic bulletin & review.

[22]  I. Pepperberg Grey Parrot (Psittacus erithacus) numerical abilities: addition and further experiments on a zero-like concept. , 2006, Journal of comparative psychology.

[23]  Worms under cover: relationships between performance in learning tasks and personality in great tits (Parus major) , 2012, Animal Cognition.

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

[25]  E. Spelke,et al.  Evolutionary and developmental foundations of human knowledge , 2004 .

[26]  Frank H. Durgin,et al.  Texture density adaptation and the perceived numerosity and distribution of texture. , 1995 .

[27]  Juan D. Delius,et al.  Beyond sensation : visual cognition in pigeons , 1993 .

[28]  M. Beran The Evolutionary and Developmental Foundations of Mathematics , 2008, PLoS biology.

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

[30]  K. van Oers,et al.  Personality predicts the use of social information. , 2010, Ecology letters.

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

[32]  J. Cantlon,et al.  Shared System for Ordering Small and Large Numbers in Monkeys and Humans , 2006, Psychological science.

[33]  Bert Reynvoet,et al.  The Role of Visual Information in Numerosity Estimation , 2012, PloS one.

[34]  Giorgio Vallortigara,et al.  Arithmetic in newborn chicks , 2009, Proceedings of the Royal Society B: Biological Sciences.

[35]  A. Bisazza,et al.  Large Number Discrimination by Mosquitofish , 2010, PLoS ONE.

[36]  J. Tautz,et al.  Number-Based Visual Generalisation in the Honeybee , 2009, PloS one.

[37]  Marco Dadda,et al.  A new training procedure for studying discrimination learning in fish , 2012, Behavioural Brain Research.

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

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

[40]  Giorgio Vallortigara,et al.  Rudimental numerical competence in 5-day-old domestic chicks (Gallus gallus): identification of ordinal position. , 2007, Journal of experimental psychology. Animal behavior processes.

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

[42]  R. Gerlai,et al.  Associative learning in zebrafish (Danio rerio) in the plus maze , 2010, Behavioural Brain Research.

[43]  Dirk Steinke,et al.  Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using ESTs , 2006, Journal of Molecular Evolution.

[44]  Andrew Sih,et al.  Behavioral syndromes: an ecological and evolutionary overview. , 2004, Trends in ecology & evolution.

[45]  T. Matsuzawa Symbolic representation of number in chimpanzees , 2009, Current Opinion in Neurobiology.

[46]  Lynne U. Sneddon,et al.  The bold and the shy: individual differences in rainbow trout , 2003 .

[47]  M. Dadda,et al.  Discrimination of the larger shoal in the poeciliid fish Girardinus falcatus , 2007 .

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

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

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

[51]  H S Terrace,et al.  Ordering of the numerosities 1 to 9 by monkeys. , 1998, Science.

[52]  Karen Wynn,et al.  Infants’ auditory enumeration: Evidence for analog magnitudes in the small number range , 2009, Cognition.

[53]  C. Uller,et al.  Horses (Equus caballus) select the greater of two quantities in small numerical contrasts , 2009, Animal Cognition.

[54]  Elizabeth M Brannon,et al.  How much does number matter to a monkey (Macaca mulatta)? , 2007, Journal of experimental psychology. Animal behavior processes.

[55]  Christian Agrillo,et al.  The Importance of Replication in Comparative Psychology: The Lesson of Elephant Quantity Judgments , 2012, Front. Psychology.

[56]  Alain Content,et al.  Judgement of discrete and continuous quantity in adults: Number counts! , 2012, Quarterly journal of experimental psychology.

[57]  Sasha R. X. Dall,et al.  The behavioural ecology of personality: consistent individual differences from an adaptive perspective , 2004 .

[58]  Jüri Allik,et al.  Interactions between area and numerosity , 1988, Psychological research.

[59]  W. Roberts Distance and magnitude effects in sequential number discrimination by pigeons. , 2010, Journal of experimental psychology. Animal behavior processes.

[60]  Michael J Beran,et al.  Chimpanzees (Pan troglodytes) respond to nonvisible sets after one-by-one addition and removal of items. , 2004, Journal of comparative psychology.

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

[62]  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.

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