Animal Cognition

, Volume 22, Issue 2, pp 223–230 | Cite as

Discrimination of group numerousness under predation risk in anuran tadpoles

  • Alessandro Balestrieri
  • Andrea GazzolaEmail author
  • Daniele Pellitteri-Rosa
  • Giorgio Vallortigara
Original Paper


For social animals, group size discrimination may play a major role in setting the trade-off between the costs and benefits of membership. Several anuran tadpoles show different degrees of social aggregation when exposed to the risk of predation. Despite the importance of aggregative behaviour as an anti-predatory response, the mechanism underlying tadpole choice of the group to join to has not been sufficiently investigated. To establish whether visual cues provide sufficient information to enable tadpoles to choose between aggregations differing in size, we explored the abilities of the larvae of two anuran species (green toad Bufotes balearicus and edible frog Pelophylax esculentus) to discriminate among four numerical combinations of conspecific tadpoles (1 vs. 4, 3 vs. 4, 4 vs. 6 and 4 vs. 8), either in the presence or absence of predatory cues. Our results suggest that in anuran larvae the capacity to discriminate between quantities is limited to small numbers (1 vs. 4 for B. balearicus and both 1 vs. 4 and 3 vs. 4 for P. esculentus). Predator-exposed toad tadpoles stayed longer close to the larger group, supporting aggregation as a major anti-predator behaviour in bufonids, while frog tadpoles showed a preference for the smaller groups, though in predator-free trials only, probably associated with lower intra-specific competition.


Aggregation Bufotes balearicus Numerical abilities Pelophylax esculentus Amphibians 



We are grateful to Prof. Francesco Bracco and to the Botanic Garden of Pavia for providing the laboratory for behavioural experiments. In particular, we are grateful to Prof. Solveig Tosi for her enthusiastic and sincere care which allowed us to perform the experiments in a supporting environment. We also thank Paolo Cauzzi for his useful suggestions. A heartfelt thanks to Leonardo and Tommaso Pellitteri-Rosa for their nice and funny help during tadpole field collection.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. The permits to perform this study were obtained from the Italian Ministry of Environment, Land and Sea (0006075–23/03/2018—PNM).

Supplementary material

10071_2019_1238_MOESM1_ESM.xlsx (15 kb)
Supplementary material 1 (XLSX 15 KB)


  1. Agrillo C, Dadda M, Serena G, Bisazza A (2008) Do fish count? Spontaneous discrimination of quantity in female mosquitofish. Anim Cogn 11:495–503. Google Scholar
  2. Agrillo C, Piffer L, Bisazza A (2011) Number versus continuous quantity in numerosity judgments by fish. Cognition 119:281–287. Google Scholar
  3. Agrillo C, Piffer L, Bisazza A, Butterworth B (2012) Evidence for two numerical systems that are similar in humans and guppies. PLoS One 7(2):e31923. Google Scholar
  4. Bennett AM, Pereira D, Murray DL (2013) Investment into defensive traits by anuran prey (Lithobates pipiens) is mediated by the starvation-predation risk trade-off. PLoS One 8(12):e82344Google Scholar
  5. Benson-Amram S, Heinen VK, Dryer SL, Holekamp KE (2011) Numerical assessment and individual call discrimination by wild spotted hyaenas, Crocuta crocuta. Anim Behav 82:743–752. Google Scholar
  6. Bertamini M, Guest M, Vallortigara G, Rugani R, Regolin L (2018) The effect of clustering on perceived quantity in humans (Homo sapiens) and in chicks (Gallus gallus). J Comp Psychol 132:280–293Google Scholar
  7. Bisazza A, De Santi A, Bonso S, Sovrano VA (2002) Frogs and toads in front of a mirror: lateralisation of response to social stimuli in tadpoles of five anuran species. Behav Brain Res 134:417–424Google Scholar
  8. Bisazza A, Piffer L, Serena G, Agrillo C (2010) Ontogeny of numerical abilities in fish. PLoS One 5(11):e15516Google Scholar
  9. Blaustein AR, O’Hara RK (1982) Kin recognition cues in Rana cascadae tadpoles. Behav Neural Biol 36:77–87Google Scholar
  10. Blaustein AR, O’Hara RK (1986) Kin recognition in tadpoles. Sci Am 254:108–116Google Scholar
  11. Blaustein AR, Waldman B (1992) Kin recognition in anuran amphibians. Anim Behav 44:207–221Google Scholar
  12. Blaustein AR, Walls SC (1995) Aggregation and kin recognition. In: Heatwole H, Sullivan BK (eds) Amphibian biology, Social behaviour, vol 2. Surrey Beatty and Sons, New South Wales, pp 568–602Google Scholar
  13. Bogale BA, Aoyama M, Sugita S (2014) Spontaneous discrimination of food quantities in the jungle crow, Corvus macrorhynchos. Anim Behav 94:73e78Google Scholar
  14. Brown RM, Taylor DH (1995) Performance and maneuvering behavior through larval ontogeny of the wood frog, Rana sylvatica. Copeia 1:1–7Google Scholar
  15. Buckingham JN, Wong BBM, Rosenthal GG (2007) Shoaling decisions in female swordtails: how do fish gauge group size? Behaviour 144:1333–1346Google Scholar
  16. Carazo P, Font E, Forteza-Behrendt E, Desfilis E (2009) Quantity discrimination in Tenebrio molitor: evidence of numerosity discrimination in an invertebrate? Anim Cogn 12:463–470. Google Scholar
  17. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator/prey interactions: a review and prospectus. Écoscience 5:338–352Google Scholar
  18. Cresswell W (1994) Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Anim Behav 47:433–442Google Scholar
  19. Cresswell W, Quinn JL (2004) Faced with a choice, sparrow hawks more often attack the more vulnerable prey group. Oikos 104:71–76Google Scholar
  20. Cresswell W, Hilton GM, Ruxton GD (2000) Evidence for a rule governing the avoidance of superfluous escape flights. Proc R Soc Lond B 267:733–737Google Scholar
  21. Cross FR, Jackson RR (2017) Representation of different exact numbers of prey by a spider-eating predator. Interf Focus 7(3):20160035Google Scholar
  22. Dacke M, Srinivasan MV (2008) Evidence for counting in insects. Anim Cogn 11:683–689. Google Scholar
  23. Feigenson L, Carey S, Hauser M (2002) The representations underlying infants’ choice of more: object files versus analog magnitudes. Psychol Sci 13(2):150–156Google Scholar
  24. Feigenson L, Dehaene S, Spelke E (2004) Core systems of number. Trends Cogn Sci 8(7):307–314Google Scholar
  25. Forsatkar MN, Nematollahi MA, Bisazza A (2016) Quantity discrimination in parental fish: female convict cichlid discriminate fry shoals of different sizes. Anim Cogn 19:959–964Google Scholar
  26. Forsman JT, Hjernquist MB, Taipale J, Gustafsson L (2008) Competitor density cues for habitat quality facilitating habitat selection and investment decisions. Behav Ecol 19:539–545. Google Scholar
  27. Foster MS, McDiarmid RW (1982) Study of aggregative behavior of Rhinophrynus dorsalis tadpoles: design and analysis. Herpetologica 38:395–404Google Scholar
  28. Gallistel CR, Gelman R (2000) Non-verbal numerical cognition: from reals to integers. Trends Cogn Sci 4(2):59–65Google Scholar
  29. Gazzola A, Van Buskirk J (2015) Isocline analysis of competition predicts stable coexistence of two amphibians. Oecologia 178:153–159. Google Scholar
  30. Gazzola A, Sacchi R, Ghitti M, Balestrieri A (2018a) The effect of thinning and cue: density ratio on risk perception by Rana dalmatina tadpoles. Hydrobiologia 813:75–83Google Scholar
  31. Gazzola A, Vallortigara G, Pellitteri-Rosa D (2018b) Continuous and discrete quantity discrimination in tortoises. Biol Lett 14:20180649. Google Scholar
  32. Glos J, Erdmann G, Dausmann KH, Linsenmair KE (2007) A comparative study of predator-induced social aggregation of tadpoles in two anuran species from western Madagascar. Herpetol J 17:261–268Google Scholar
  33. Gómez-Laplaza LM, Gerlai R (2011) Spontaneous discrimination of small quantities: shoaling preferences in angelfish (Pterophyllum scalare). Anim Cogn 14:565–574. Google Scholar
  34. Gómez-Laplaza LM, Gerlai R (2013) Quantification abilities in angelfish (Pterophyllum scalare): the influence of continuous variables. Anim Cogn 16:373–383Google Scholar
  35. Griffiths RA, Foster JP (1998) The effect of social interactions on tadpole activity and growth in the British anuran amphibians (Bufo bufo, B. calamita, and Rana temporaria). J Zool (London) 245:431–437Google Scholar
  36. Hettyey A, Zoltán T, Thonhauser EK, Frommen JG, Penn DJ, Van Buskirk J (2015) The relative importance of prey-borne and predator-borne chemical cues for inducible antipredator responses in tadpoles. Oecologia 79:699–710Google Scholar
  37. Hoare DJ, Couzin ID, Godin JGJ, Krause J (2004) Context-dependent group size choice in fish. Anim Behav 67:155–164. Google Scholar
  38. Howard S, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (2018) Numerical ordering of zero in honeybees. Science 360:1124–1126. Google Scholar
  39. Irie-Sugimoto N, Kobayashi T, Sato T, Hasegawa T (2009) Relative quantity judgment by Asian elephants (Elephas maximus). Anim Cogn 12(1):193–199Google Scholar
  40. Kishida O, Nishimura K (2005) Multiple inducible defences against multiple predators in the anuran tadpoles, Rana pirica. Evol Ecol Res 7:619–631Google Scholar
  41. Kloke JD, McKean JW (2012) Rfit: rank-based estimation for linear models. The R Journal 4(2):57–64Google Scholar
  42. Krause J, Ruxton GD (2002) Living in groups. Oxford series in ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  43. Krause J, Ruxton GD, Rubenstein D (1998) Is there always an influence of shoal size on predator hunting success? J Fish Biol 52:494–501Google Scholar
  44. Kruske P, Uller C, Dicke U (2010) Quantity discrimination in salamanders. J Exp Biol 213:1822–1828Google Scholar
  45. Leu ST, Whiting MJ, Mahony MJ (2013) Making friends: social attraction in larval green and golden bell frogs, Litoria aurea. PLoS One 8(2):e56460. Google Scholar
  46. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canad J Zool 68:619–640Google Scholar
  47. Lucon-Xiccato T, Miletto Petrazzini ME, Agrillo C, Bisazza A (2015) Guppies discriminate between two quantities of food items but prioritize item size over total amount. Anim Behav 107:183e191Google Scholar
  48. Lucon-Xiccato T, Gatto E, Bisazza A (2018) Quantity discrimination by treefrogs. Anim Behav 139:61–69. Google Scholar
  49. Lyon BE (2003) Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422:495–499Google Scholar
  50. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609. Google Scholar
  51. Magurran AE, Pitcher TJ (1987) Provenance, shoal size and the sociobiology of predator-evasion behaviour in minnow shoals. Proc R Soc Lond B 229:439–465Google Scholar
  52. McClure KV, Mora JW, Smith GR (2009) Effects of light and group size on the activity of wood frog tadpoles Rana sylvatica. Acta Herp 4(1):103–107Google Scholar
  53. Miletto Petrazzini ME, Fraccaroli I, Gariboldi F, Agrillo C, Bisazza A, Bertolucci C, Foa A (2017) Quantitative abilities in a reptile (Podarcis sicula). Biol Lett 13:20160899. Google Scholar
  54. Miletto Petrazzini ME, Bertolucci C, Foa A (2018) Quantity discrimination in trained lizards (Podarcis sicula). Front Psychol 9:274. Google Scholar
  55. Nelson XJ, Jackson RR (2012) The role of numerical competence in a specialized predatory strategy of an araneophagic spider. Anim Cogn 15:699–710. Google Scholar
  56. Nordell SE (1998) The response of female guppies, Poecilia reticulata, to chemical stimuli from injured conspecifics. Envir Biol Fishes 51:331–338Google Scholar
  57. O’Hara RK, Blaustein AR (1988) Hyla regilla and Rana pretiosa tadpoles fail to display kin recognition behaviour. Anim Behav 36:946–948Google Scholar
  58. Pepperberg IM (2006) Grey parrot numerical competence: a review. Anim Cogn 9:377–391. Google Scholar
  59. Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) The behavior of teleost fishes, 2nd edn. Chapman and Hall, New York, pp 363–439Google Scholar
  60. Potrich D, Sovrano VA, Stancher G, Vallortigara G (2015) Quantity discrimination by zebrafish (Danio rerio). J Comp Psychol 129:388–393Google Scholar
  61. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540Google Scholar
  62. Rugani R, Regolin L, Vallortigara G (2008) Discrimination of small numerosities in young chicks. J Exp Psychol Anim Behav Proc 34:388–399Google Scholar
  63. Rugani R, Fontanari L, Simoni E, Regolin L, Vallortigara G (2009) Arithmetic in newborn chicks. Proc R Soc Lond B 276:2451–2460Google Scholar
  64. Rugani R, Regolin L, Vallortigara G (2010) Imprinted numbers: newborn chicks’ sensitivity to number vs. continuous extent of objects they have been reared with. Dev Sci 13:790–797Google Scholar
  65. Rugani R, Regolin L, Vallortigara G (2011) Summation of large numerousness by newborn chicks. Front Psychol 2:179. Google Scholar
  66. Rugani R, Cavazzana A, Vallortigara G, Regolin L (2013a) One, two, three, four, or is there something more? Numerical discrimination in day-old domestic chicks. Anim Cogn 16:557–564Google Scholar
  67. Rugani R, Vallortigara G, Regolin L (2013b) Numerical abstraction in young domestic chicks (Gallus gallus). PLoS One 8(6):e65262. Google Scholar
  68. Rugani R, Vallortigara G, Regolin G (2014) From small to large: numerical discrimination by young domestic chicks (Gallus gallus). J Comp Psychol 128:163–171Google Scholar
  69. Rugani R, McCrink K, de Hevia M-D, Vallortigara G, Regolin L (2016) Ratio abstraction over discrete magnitudes by newly hatched domestic chicks (Gallus gallus). Sci Rep 6:30114. Google Scholar
  70. Semlitsch RD (1990) Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Can J Zool 68:1027–1030Google Scholar
  71. Spieler M, Linsenmair KE (1999) Aggregation behaviour of Bufo maculatus tadpoles as an antipredator mechanism. Ethology 105:665–686. Google Scholar
  72. Stancher G, Sovrano VA, Potrich D, Vallortigara G (2013) Discrimination of small quantities by fish (redtail splitfin, Xenotoca eiseni). Anim Cogn 16:307–312Google Scholar
  73. Stancher G, Rugani R, Regolin L, Vallortigara G (2015) Numerical discrimination by frogs (Bombina orientalis). Anim Cogn 18:219–229. Google Scholar
  74. Stav G, Kotler BP, Blaustein L (2007) Direct and indirect effects of dragonfly (Anax imperator) nymphs on green toad (Bufo viridis) tadpoles. Hydrobiologia 579:85–93Google Scholar
  75. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  76. Trick LM, Pylyshyn ZW (1994) Why are small and large numbers enumerated differently? A limited-capacity preattentive stage in vision. Psychol Rev 101:80–102Google Scholar
  77. Uller C, Carey S, Huntley-Fenner G, Klatt L (1999) What representations might underlie infant numerical knowledge. Cogn Dev 14:1–36Google Scholar
  78. Uller C, Jaeger R, Guidry G, Martin C (2003) Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian. Anim Cogn 6:105–112. Google Scholar
  79. Vallortigara G (2014) Foundations of number and space representations in non-human species. In: Geary DC, Bearch DB, Mann Koepke K (eds) Evolutionary origins and early development of number processing. Elsevier, New York, pp 35–66Google Scholar
  80. Vallortigara G (2017) An animal’s sense of number. In: Adams JW, Barmby P, Alex M (eds) The nature and development of mathematics. Taylor and Francis, Oxon, pp 43–65Google Scholar
  81. Vallortigara G (2018) Comparative cognition of number and space: the case of geometry and of the mental number line. Philos Trans R Soc B 373:20170120. Google Scholar
  82. Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489Google Scholar
  83. Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585Google Scholar
  84. Van Buskirk J, Ferrari M, Kueng D, Näpflin K, Ritter N (2011) Prey risk assessment depends on conspecific density. Oikos 120:1235–1239Google Scholar
  85. Van Buskirk J, Krugel A, Kunz J, Miss F, Stamm A (2014) The rate of degradation of chemical cues indicating predation risk: an experiment and review. Ethology 120:942–949Google Scholar
  86. vanMarle K, Wynn K (2011) Tracking and quantifying objects and non-cohesive substances. Dev Sci 14(3):502–515Google Scholar
  87. Vonk J, Beran MJ (2012) Bears “count” too: quantity estimation and comparison in black bears, Ursus americanus. Anim Behav 84:231–238. Google Scholar
  88. Vonk J, Torgerson-White L, McGuire M, Thueme M, Thomas J, Beran MJ (2014) Quantity estimation and comparison in western lowland gorillas (Gorilla gorilla gorilla). Anim Cogn 17:755–765. Google Scholar
  89. Waldman B (1991) Kin recognition in amphibians. In: Hepper PG (ed) Kin recognition. Cambridge University Press, Cambridge, pp 162–219Google Scholar
  90. Wassersug RJ, Hessler CM (1971) Tadpole behaviour: aggregation in larval Xenopus laevis. Anim Behav 19:386–389Google Scholar
  91. Watt PJ, Nottingham SF, Young S (1997) Toad tadpole aggregation behaviour: evidence for a predator avoidance function. Anim Behav 54:865–872Google Scholar
  92. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoGoogle Scholar
  93. Xiong W, Yi L-C, Tang Z, Zhao X, Fu S-J (2018) Quantity discrimination in fish species: fish use non-numerical continuous quantity traits to select shoals. Anim Cogn. Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Earth and Environmental SciencesUniversity of PaviaPaviaItaly
  2. 2.Center for Mind/Brain SciencesUniversity of TrentoRoveretoItaly

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