Animal Cognition

, Volume 12, Issue 3, pp 463–470 | Cite as

Quantity discrimination in Tenebrio molitor: evidence of numerosity discrimination in an invertebrate?

  • P. Carazo
  • E. Font
  • E. Forteza-Behrendt
  • E. Desfilis
Original Paper


Numerosity discrimination, the ability to distinguish between sets with more and less items, is recognised as the foundation for higher numerical abilities. Understanding numerosity discrimination from a comparative perspective is hence pivotal in tracing the evolution of numerical representation systems. However, numerosity discrimination has been well studied only in vertebrates, where two innate systems of number representation have been described: an ‘analog magnitude system’ used to discriminate among numerosities by representing them as cardinal magnitudes and a ‘parallel individualisation system’ that allows precise discrimination among small arrays of items (≤4) by representing objects individually. We investigated the existence of quantity discrimination in an insect species (Tenebrio molitor) by using a spontaneous two-choice procedure in which males were exposed to substrates bearing odours from different numbers of females (≤4) in increasing numerosity ratios (1:4, 1:3 and 1:2). We show that males can discriminate sources of odours reflecting 1 versus 4 and 1 versus 3 females, but not 2 versus 4 or 1 versus 2, indicating that T. molitor males exhibit a marked preference for sources reflecting more female donors only when numerosity ratios are below 1:2. We discuss the functional significance of this finding and whether our pattern of results could be best explained by summation of a non-numerical continuous variable or by the existence of a numerosity discrimination mechanism with an operational signature ratio of 1:2.


Numerosity discrimination Tenebrio molitor Invertebrate Chemical communication 



We are grateful to M.D. Hauser, R. Menzel and three anonymous referees for their insightful criticisms and comments on a previous version of this manuscript. We also wish to thank Carlos Sampedro for his help in the maintenance of insect cultures. P.C. was supported by a research grant (FPU) from the Ministerio de Educación y Ciencia of Spain.


  1. Agrillo C, Dadda M (2007) Discrimination of the larger shoal in the poeciliid fish Girardinus falcatus. Ethol Ecol & Evol 19:145–157Google Scholar
  2. Agrillo C, Dadda M, Bisazza A (2007) Quantity discrimination in female mosquitofish. Anim Cogn 10:63–70PubMedCrossRefGoogle Scholar
  3. Barner D, Wood J, Hauser M, Carey S (2008) Evidence for a non-linguistic distinction between singular and plural sets in rhesus monkeys. Cognition 107:603–622PubMedCrossRefGoogle Scholar
  4. Beauchamp G (2003) Group-size effects on vigilance: a search for mechanisms. Behav Proc 63:111–121CrossRefGoogle Scholar
  5. Bekoff M, Allen C, Burghardt GM (2002) The cognitive animal: empirical and theoretical perspectives on animal cognition. The MIT Press, CambridgeGoogle Scholar
  6. Bhattacharya AK, Ameel JJ, Waldbauer GP (1970) A method for sexing living pupal and adult yellow mealworms. Ann Entomol Soc Am 63:1783Google Scholar
  7. Boisvert MJ, Sherry DF (2006) Interval timing by an invertebrate, the bumble bee Bombus impatiens. Curr Biol 16:1636–1640PubMedCrossRefGoogle Scholar
  8. Brannon EM, Terrace HS (2002) The evolution and ontogeny of ordinal numerical ability. In: Bekoff M, Allen C, Burghardt GM (eds) The cognitive animal: empirical and theoretical perspectives on animal cognition. The MIT Press, Cambridge, pp 197–204Google Scholar
  9. Brown WD (1990) Size-assortative mating in the blister beetle Lytta magister (Coleoptera: meloidae) is due to male and female preference for larger mates. Anim Behav 40:901–909CrossRefGoogle Scholar
  10. Buckingham JN, Wong BBM, Rosenthal GG (2007) Shoaling decisions in female swordtails: how do fish gauge group size? Behaviour 144:1333–1346CrossRefGoogle Scholar
  11. Butterworth B (1999) The mathematical brain. Macmillan, LondonGoogle Scholar
  12. Carazo P, Sanchez E, Font E, Desfilis E (2004) Chemosensory cues allow male Tenebrio molitor beetles to asses the reproductive status of potential mates. Anim Behav 68:123–129CrossRefGoogle Scholar
  13. Carazo P, Font E, Alfthan B (2007) Chemical assessment of sperm competition levels and the evolution of internal spermatophore guarding. Proc R Soc B 274:261–267PubMedCrossRefGoogle Scholar
  14. Chen L, Zhang S, Srinivasan MV (2003) Global perception in small brains: topological pattern recognition in honey bees. PNAS 100:6884–6889PubMedCrossRefGoogle Scholar
  15. Chittka L, Brockmann A (2005) Perception space—the final frontier. PLoS Biol 3:0564–0568CrossRefGoogle Scholar
  16. Chittka L, Geiger K (1995) Can honey bees count landmarks? Anim Behav 49:159–164CrossRefGoogle Scholar
  17. Cleveland WS (1993) Visualizing data. Hobart Press, SummitGoogle Scholar
  18. D’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174PubMedCrossRefGoogle Scholar
  19. Dacke M, Srinivasan MV (2008) Evidence for counting in insects. Anim Cogn 11:683–689PubMedCrossRefGoogle Scholar
  20. Dehaene S (1997) The number sense: how the mind creates mathematics. Oxford University Press, OxfordGoogle Scholar
  21. Dehaene S, Dehaene-Lambertz G, Cohen L (1998) Abstract representations of numbers in the animal and human brain. TINS 21:355–361PubMedGoogle Scholar
  22. Drnevich JM (2003) Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor L. Anim Behav 66:349–357CrossRefGoogle Scholar
  23. Drnevich JM, Hayes EF, Rutowski RL (2000) Sperm precedence, mating interval and a novel mechanism of paternity bias in a beetle (Tenebrio molitor L.). Behav Ecol Sociobiol 48:447–451CrossRefGoogle Scholar
  24. Farnsworth GL, Smolinski JL (2006) Numerical discrimination by wild northern mockingbirds. Condor 108:953–957CrossRefGoogle Scholar
  25. Feigenson L, Dehaene S, Spelke E (2004) Core systems of number. TICS 8:307–314Google Scholar
  26. Ferkin MH, Pierce AA, Sealand RO, delBarco-Trillo J (2005) Meadow voles, Microtus pennsylvanicus, can distinguish more over-marks from fewer over-marks. Anim Cogn 8:182–189PubMedCrossRefGoogle Scholar
  27. Franks NR, Dornhaus A, Metherell BG, Nelson TR, Lanfear SA, Symes WS (2006) Not everything that counts can be counted: ants use multiple metrics for a single nest trait. Proc R Soc B 273:165–169PubMedCrossRefGoogle Scholar
  28. Gage MJG, Baker RR (1991) Ejaculate size varies with socio-sexual situation in an insect. Ecol Entomol 16:331–337CrossRefGoogle Scholar
  29. Gallistel CR, Gelman R (2000) Non-verbal numerical cognition: from the reals to the integers. TICS 4:59–65Google Scholar
  30. Griffith OL (2001) The effect of mating on the pheromone system of the yellow mealworm beetle, Tenebrio molitor. Honours Thesis, University of WinnipegGoogle Scholar
  31. Happ GM (1969) Multiple sex pheromones of the mealworm beetle, Tenebrio molitor L. Nature 222:180–181PubMedCrossRefGoogle Scholar
  32. Happ GM, Wheeler J (1969) Bioassay, preliminary purification and effect of age, crowding and mating in the release of sex pheromone by female Tenebrio molitor. Ann Entomol Soc Am 62:846–851Google Scholar
  33. Hauser M (2000) What do animals think about numbers? Am Sci 88:76–83Google Scholar
  34. Hauser MD, Spelke E (2004) Evolutionary and developmental foundations of human knowledge: a case study of mathematics. In: Gazzaniga MS (ed) The cognitive neurosciences III. The MIT Press, Cambridge, pp 853–864Google Scholar
  35. Hauser MD, Carey S, Hauser LB (2000) Spontaneous number representation in semi-free-ranging rhesus monkeys. Proc R Soc Lond B 267:829–833CrossRefGoogle Scholar
  36. Hauser MD, Tsao F, Garcia P, Spelke E (2003) Evolutionary foundations of number: spontaneous representation of numerical magnitudes by cotton-top tamarins. Proc R Soc Lond B 270:1441–1446CrossRefGoogle Scholar
  37. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70Google Scholar
  38. Honig WK, Stewart KE (1989) Discrimination of relative numerosity by pigeons. Anim Learn Behav 17:134–146Google Scholar
  39. Karban R, Black CA, Weinbaum SA (2000) How 17-year cicadas keep track of time. Ecol Let 3:253–256CrossRefGoogle Scholar
  40. Lipton JS, Spelke ES (2003) Origins of number sense: large-number discrimination in human infants. Psych Sci 14:396–401CrossRefGoogle Scholar
  41. Lyon BE (2003) Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422:495–499PubMedCrossRefGoogle Scholar
  42. McComb K, Packer C, Pusey A (1994) Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Anim Behav 47:379–387CrossRefGoogle Scholar
  43. Meck WH, Church RM (1983) A mode control model of counting and timing processes. J Exp Psychol Anim Behav Process 9:320–334PubMedCrossRefGoogle Scholar
  44. Meck WH, Church RM, Gibbon J (1985) Temporal integration in duration and number discrimination. J Exp Psychol Anim Behav Process 11:591–597PubMedCrossRefGoogle Scholar
  45. Menzel R, Brembs B, Giurfa M (2007) Cognition in invertebrates. In: Strausfeld NJ, Bullock TH (eds) Evolution of nervous systems in invertebrates, vol 11. Elsevier, Amsterdam, pp 403–442Google Scholar
  46. Moyer RS, Landauer TK (1967) Time required for judgements of numerical inequality. Nature 215:1519–1520PubMedCrossRefGoogle Scholar
  47. Pepperberg IM (2006) Grey parrot numerical competence: a review. Anim Cogn 9:377–391PubMedCrossRefGoogle Scholar
  48. Rantala MJ, Kortet R, Kotiaho JS, Vainikka A, Suhonen J (2003) Condition dependence of pheromones and immune function in the grain beetle Tenebrio molitor. Func Ecol 17:534–540CrossRefGoogle Scholar
  49. Roberts W (1997) Principles of animal cognition. McGraw-Hill, New YorkGoogle Scholar
  50. Rugani R, Regolin L, Vallortigara G (2007) Rudimental numerical competence in 5-day-old domestic chicks (Gallus gallus): identification of ordinal position. J Exp Psych 33:21–31Google Scholar
  51. Shettleworth SJ (1998) Cognition, evolution and behaviour. Oxford University Press, OxfordGoogle Scholar
  52. Siegel S, Castellan NJJ (1989) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New YorkGoogle Scholar
  53. Skorupski P, Chittka L (2006) Animal cognition: an insect’s sense of time? Curr Biol 16:1636–1640CrossRefGoogle Scholar
  54. Tanaka Y, Honda H, Ohsawa K, Yamamoto I (1986) A sex attractant of the yellow mealworm, Tenebrio molitor L. and its role in the mating behavior. J Pesticide Sci 11:49–55Google Scholar
  55. Tegeder RW, Krause J (1995) Density dependence and numerosity in fright stimulated aggregation behaviour of shoaling fish. Phil Trans R Soc Lond B 350:381–390CrossRefGoogle Scholar
  56. Thom MD, Hurst JL (2004) Individual recognition by scent. Ann Zool Fennici 41:765–787Google Scholar
  57. Thomas ML, Simmons LW (2009) Male-derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets. Proc R Soc B 276:383–388PubMedCrossRefGoogle Scholar
  58. Trick LM, Pylyshyn ZW (1994) Why are small and large numbers enumerated differently? A limited-capacity preattentive stage in vision. Psychol Rev 101:80–102PubMedCrossRefGoogle Scholar
  59. Tschinkel W, Willson C, Bern HA (1967) Sex pheromone of the mealworm beetle (Tenebrio molitor). J Exp Zool 164:81–86PubMedCrossRefGoogle Scholar
  60. Uller C, Jaeger R, Guidry G, Martin C (2003) Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian. Anim Cogn 6:105–112PubMedGoogle Scholar
  61. Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312:1965–1967PubMedCrossRefGoogle Scholar
  62. Worden BD, Parker PG, Pappas PW (2000) Parasites reduce attractiveness and reproductive success in male grain beetles. Anim Behav 59:543–550PubMedCrossRefGoogle Scholar
  63. Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, CambridgeGoogle Scholar
  64. Wynn K (1998) Psychological foundations of number: numerical competence in human infants. TICS 2:296–302Google Scholar
  65. Xu F (2003) Numerosity discrimination in infants: evidence for two systems of representations. Cognition 89:B15–B25PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • P. Carazo
    • 1
  • E. Font
    • 1
  • E. Forteza-Behrendt
    • 1
  • E. Desfilis
    • 2
  1. 1.Instituto Cavanilles de Biodiversidad y Biología EvolutivaUniversidad de ValenciaValenciaSpain
  2. 2.Departamento de PsicobiologíaUniversidad Complutense de MadridMadridSpain

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