Exclusion in the field: wild brown skuas find hidden food in the absence of visual information

Abstract

Inferential reasoning by exclusion allows responding adaptively to various environmental stimuli when confronted with inconsistent or partial information. In the experimental context, this mechanism involves selecting correctly between an empty option and a potentially rewarded one. Recently, the increasing reports of this capacity in phylogenetically distant species have led to the assumption that reasoning by exclusion is the result of convergent evolution. Within one largely unstudied avian order, i.e. the Charadriiformes, brown skuas (Catharacta antarctica ssp lonnbergi) are highly flexible and opportunistic predators. Behavioural flexibility, along with specific aspects of skuas’ feeding ecology, may act as influencing factors in their ability to show exclusion performance. Our study aims to test whether skuas are able to choose by exclusion in a visual two-way object-choice task. Twenty-six wild birds were presented with two opaque cups, one covering a food reward. Three conditions were used: ‘full information’ (showing the content of both cups), ‘exclusion’ (showing the content of the empty cup), and ‘control’ (not showing any content). Skuas preferentially selected the rewarded cup in the full information and exclusion condition. The use of olfactory cues was excluded by results in the control condition. Our study opens new field investigations for testing further the cognition of this predatory seabird.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aust U, Range F, Steurer M, Huber L (2008) Inferential reasoning by exclusion in pigeons, dogs, and humans. Anim Cogn 11:587–597

    PubMed  Article  Google Scholar 

  2. Burton RW (1968) Breeding biology of the brown skua, Catharacta skua lonnbergi (Mathews), at Signy Island, South Orkney Islands. Br Antarct Surv B 15:9–28

    Google Scholar 

  3. Byrne RW, Bates LA (2011) Cognition in the wild: exploring animal minds with observational evidence. Biol Lett 7:619–622

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. Call J (2004) Inferences about the location of food in the great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus). J Comp Psychol 118:232–241

    PubMed  Article  Google Scholar 

  5. Call J (2006) Inferences by exclusion in the great apes: the effect of age and species. Anim Cogn 9:393–403

    PubMed  Article  Google Scholar 

  6. Carneiro APB, Manica A, Phillips RA (2014) Foraging behaviour and habitat use by brown skuas Stercorarius lonnbergi breeding at South Georgia. Mar Biol 161:1755–1764

    Article  Google Scholar 

  7. Carneiro AP, Manica A, Trivelpiece WZ, Phillips RA (2015) Flexibility in foraging strategies of Brown Skuas in response to local and seasonal dietary constraints. J Ornithol 156:625–633

    Article  Google Scholar 

  8. Cauchoix M, Hermer E, Chaine AS, Morand-Ferron J (2017) Cognition in the field: comparison of reversal learning performance in captive and wild passerines. Sci Rep 7:1–10

    CAS  Article  Google Scholar 

  9. Chester SR (1993) Antarctic birds and seals. Wandering Albatross, San Mateo

    Google Scholar 

  10. Danel S, von Bayern AM, Osiurak F (2019) Ground-hornbills (Bucorvus) show means-end understanding in a horizontal two-string discrimination task. J Ethol 37:117–122

    Article  Google Scholar 

  11. Darmaillacq AS, Dickel L, Avargues-Weber A, Duboscq J, Dufour V, Jozet-Alves C (2018) Cognition animale: perception, raisonnement et représentations. Dunod

  12. De Kort SR, Clayton NS (2006) An evolutionary perspective on caching by corvids. Proc R Soc B 273:417–423

    PubMed  Article  Google Scholar 

  13. Erdőhegyi Á, Topál J, Virányi Z, Miklósi Á (2007) Dog-logic: inferential reasoning in a two-way choice task and its restricted use. Anim Behav 74:725–737

    Article  Google Scholar 

  14. Fokkema M, Smits N, Zeileis A, Hothorn T, Kelderman H (2018) Detecting treatment-subgroup interactions in clustered data with generalized linear mixed-effects model tree. Behav Res Methods 50:2016–2034

    CAS  PubMed  Article  Google Scholar 

  15. Furness RW (1987) The Skuas. Pyser Press, Carlton

    Google Scholar 

  16. Furness RW, Boesman P, Garcia EFJ (2018) The brown skua (Catharacta antarctica). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

  17. Gagne M, Levesque K, Nutile L, Locurto C (2012) Performance on patterned string problems by common marmosets (Callithrix jacchus). Anim Cogn 15:1021–1030

    PubMed  PubMed Central  Article  Google Scholar 

  18. Gajdon GK, Fijn N, Huber L (2006) Limited spread of innovation in a wild parrot, the kea (Nestor notabilis). Anim Cogn 9:173–181

  19. Garland A, Low J, Armstrong N, Burns KC (2014) Wild robins (Petroica longipes) respond to human gaze. Anim Cogn 17:1149–1156

    PubMed  Article  Google Scholar 

  20. Grant PB, Samways MJ (2015) Acoustic prey and a listening predator: interaction between calling katydids and the bat-eared fox. Bioacoustics 24:49–61

    Article  Google Scholar 

  21. Grether WF, Maslow AH (1937) An experimental study of insight in monkeys. J Comp Psychol 24:127–134

    Article  Google Scholar 

  22. Hahn S, Peter HU (2003) Feeding territoriality and the reproductive consequences in brown skuas Catharacta antarctica lonnbergi. Polar Biol 26:552–559

    Article  Google Scholar 

  23. Hill A, Collier-Baker E, Suddendorf T (2011) Inferential reasoning by exclusion in great apes, lesser apes, and spider monkeys. J Comp Psychol 125:91–103

    PubMed  Article  Google Scholar 

  24. Hill A, Collier-Baker E, Suddendorf T (2012) Inferential reasoning by exclusion in children (Homo sapiens). J Comp Psychol 126:243–254

    PubMed  Article  Google Scholar 

  25. Jacobs IF, Osvath M (2015) The string-pulling paradigm in comparative psychology. J Comp Psychol 129:89–120

  26. Jelbert SA, Taylor AH, Gray RD (2015) Reasoning by exclusion in New Caledonian crows (Corvus moneduloides) cannot be explained by avoidance of empty containers. J Comp Psychol 129:283–290

    PubMed  Article  Google Scholar 

  27. Ketchaisri O, Siripunkaw C, Plotnik JM (2019) The use of a human’s location and social cues by Asian elephants in an object-choice task. Anim Cogn 22:907–915

    PubMed  Article  Google Scholar 

  28. Lee WY, Han YD, Jablonski PG, Jung JW, Kim JH (2016) Antarctic skuas recognize individual humans. Anim Cogn 19:861–865

    PubMed  Article  Google Scholar 

  29. Maille A, Roeder JJ (2012) Inferences about the location of food in lemurs (Eulemur macaco and Eulemur fulvus): a comparison with apes and monkeys. Anim Cogn 15:1075–1083

    CAS  PubMed  Article  Google Scholar 

  30. Marsh HL, Vining AQ, Levendoski EK, Judge PG (2015) Inference by Exclusion in Lion-Tailed Macaques (Macaca silenus), a Hamadryas Baboon (Papio hamadryas), Capuchins (Sapajus apella), and Squirrel Monkeys (Saimiri sciureus). J Comp Psychol 3:256–267

    Article  Google Scholar 

  31. Mikolasch S, Kotrschal K, Schloegl C (2011) African grey parrots (Psittacus erithacus) use inference by exclusion to find hidden food. Biol Lett 7:875–877

    PubMed  PubMed Central  Article  Google Scholar 

  32. Mikolasch S, Kotrschal K, Schloegl C (2012) Is caching the key to exclusion in corvids? The case of carrion crows (Corvus corone corone). Anim Cogn 15:73–82

    PubMed  Article  Google Scholar 

  33. Moncorps S, Chapuis J, Haubreux D, Bretagnolle V (1998) Diet of the Brown Skua Catharacta skua lonnbergi on the Kerguelen archipelago: comparisons between techniques and between islands. Polar Biol 19:9–16

    Article  Google Scholar 

  34. Morand-Ferron J, Sol D, Lefebvre L (2007) Food stealing in birds: brain or brawn? Anim Behav 74:1725–1734

    Article  Google Scholar 

  35. Mougeot F, Bretagnolle V (2000) Predation as a cost of sexual communication in nocturnal seabirds: an experimental approach using acoustic signals. Anim Behav 60:647–656

    CAS  PubMed  Article  Google Scholar 

  36. Mougeot F, Genevois F, Bretagnolle V (1998) Predation on burrowing petrels by the brown skua (Catharacta skua lonnbergi) at Mayes Island, Kerguelen. J Zool 244:429–438

    Google Scholar 

  37. Nawroth C, von Borell E (2015) Domestic pigs’ (Sus scrofa domestica) use of direct and indirect visual and auditory cues in an object choice task. Anim Cogn 18:757–766

    PubMed  Article  Google Scholar 

  38. Nawroth C, von Borell E, Langbein J (2014) Exclusion performance in dwarf goats (Capra aegagrus hircus) and sheep (Ovis orientalis aries). PLoS ONE 9:e93534

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  39. O’Hara M, Auersperg AM, Bugnyar T, Huber L (2015) Inference by exclusion in Goffin cockatoos (Cacatua goffini). PLoS ONE 10:e0134894

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  40. O’Hara M, Schwing R, Federspiel I, Gajdon GK, Huber L (2016) Reasoning by exclusion in the kea (Nestor notabilis). Anim Cogn 19:965–975

    PubMed  PubMed Central  Article  Google Scholar 

  41. Paukner A, Huntsberry ME, Suomi SJ (2009) Tufted capuchin monkeys (Cebus apella) spontaneously use visual but not acoustic information to find hidden food items. J Comp Psychol 123:26–33

    PubMed  PubMed Central  Article  Google Scholar 

  42. Paxton Gazes R, Chee NW, Hampton RR (2018) Monkeys choose, but do not learn, through exclusion. Anim Behav Cogn 5:1–25

    Article  Google Scholar 

  43. Penn DC, Povinelli DJ (2007) Causal cognition in human and nonhuman animals: a comparative, critical review. Annu Rev Psychol 58:97–118

    PubMed  Article  Google Scholar 

  44. Pepperberg IM, Koepke A, Livingston P, Girard M, Hartsfield LA (2013) Reasoning by inference: further studies on exclusion in grey parrots (Psittacus erithacus). J Comp Psychol 127:272–281

    PubMed  Article  Google Scholar 

  45. Petit O, Dufour V, Herrenschmidt M, De Marco A, Sterck EH, Call J (2015) Inferences about food location in three cercopithecine species: an insight into the socioecological cognition of primates. Anim Cogn 4:821–830

    Article  Google Scholar 

  46. Piaget J (1954) The construction of reality in the child. Basic Books, New York

    Google Scholar 

  47. Plotnik JM, Pokorny JJ, Keratimanochaya T, Webb C et al (2013) Visual cues given by humans are not sufficient for Asian elephants (Elephas maximus) to nd hidden food. PLoS ONE 8:e61174

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. Plotnik JM, Shaw RC, Brubaker DL, Tiller LN, Clayton SC (2014) Thinking with their trunks: elephants use smell but not sound to locate food and exclude nonrewarding alternatives. Anim Behav 88:91–98

    Article  Google Scholar 

  49. Premack D, Premack AJ (1994) Levels of causal understanding in chimpanzees and children. Cognition 50:347–362

    CAS  PubMed  Article  Google Scholar 

  50. R Core Team (2019) R: A language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  51. Rice WR (1982) Acoustic location of prey by the marsh hawk: adaptation to concealed prey. Auk 19:403–413

    Article  Google Scholar 

  52. Ricklefs RE (2004) The cognitive face of avian life histories: the 2003 Margaret Morse Nice lecture. Wilson J Ornithol 116:119–133

    Google Scholar 

  53. Romain A, Broihanne M-H, De Marco A, Ngoubangoye B, Call J, Rebout N, Dufour V (2021) Non-human primates use combined rules when deciding under ambiguity. Phil Trans R Soc B 376:20190672

    CAS  PubMed  Article  Google Scholar 

  54. Sabbatini G, Visalberghi E (2008) Inferences about the location of food in capuchin monkeys (Cebus apella) in two sensory modalities. J Comp Psychol 122:156–166

    PubMed  Article  Google Scholar 

  55. Schloegl C (2011) What you see is what you get-reloaded: can jackdaws (Corvus monedula) find hidden food through exclusion? J Comp Psychol 125:162–174

    PubMed  Article  Google Scholar 

  56. Schloegl C, Dierks A, Gajdon GK, Huber L, Kotrschal K, Bugnyar T (2009) What you see is what you get? Exclusion performances in ravens and keas. PLoS ONE 4:e6368

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  57. Schloegl C, Schmidt J, Boeckle M, Weiß BM, Kotrschal K (2012) Grey parrots use inferential reasoning based on acoustic cues alone. Proc R Soc B 279:4135–4142

    PubMed  Article  Google Scholar 

  58. Schmitt V, Fischer J (2009) Inferential reasoning and modality dependent discrimination learning in olive baboons (Papio hamadryas anubis). J Comp Psychol 123:316–325

    PubMed  Article  Google Scholar 

  59. Schreiber EA, Burger J (2002) Biology of marine birds. CRC Press, Boca Raton

    Google Scholar 

  60. Shaw RC, Plotnik JM, Clayton NS (2013) Exclusion in corvids: the performance of food-caching Eurasian jays (Garrulus glandarius). J Comp Psychol 127:428–435

    PubMed  Article  Google Scholar 

  61. Shaw RC, Boogert NJ, Clayton NS, Burns KC (2015) Wild psychometrics: evidence for ‘general’ cognitive performance in wild New Zealand robins, Petroica longipes. Anim Behav 109:101–111

    Article  Google Scholar 

  62. Sittler B, Aebischer A, Gilg O (2011) Post-breeding migration of four Long-tailed Skuas (Stercorarius longicaudus) from North and East Greenland to West Africa. J Ornithol 152:375–381

    Article  Google Scholar 

  63. Spear LB, Howell SNG, Oedekoven CS, Legay D, Bried J (1999) Kleptoparasitism by brown skuas on albatrosses and giant-petrels in the Indian ocean. Auk 116:545–548

    Article  Google Scholar 

  64. Subias L, Griffin AS, Guez D (2019) Inference by exclusion in the Red-tailed Black Cockatoo (Calyptorhynchus banksii). Integr Zool 14:193–203

    PubMed  Article  Google Scholar 

  65. Tebbich S, Seed AM, Emery NJ, Clayton NS (2007) Non-tool-using rooks, Corvus frugilegus, solve the trap-tube problem. Anim Cogn 10:225–231

    PubMed  Article  Google Scholar 

  66. Tornick JK, Gibson BM (2013) Tests of inferential reasoning by exclusion in Clark’s nutcrackers (Nucifraga columbiana). Anim Cogn 16:583–597

    PubMed  Article  Google Scholar 

  67. Trivelpiece W, Butler RG, Volkman NJ (1980) Feeding territories of Brown Skuas (Catharacta lonnbergi). Auk 97:669–676

    Google Scholar 

  68. Völter CJ and Call J (2017) Causal and inferential reasoning in animals. In J Call, GM Burghardt, IM Pepperberg, CT Snowdon, & T Zentall (Eds.), APA handbooks in psychology®. APA handbook of comparative psychology: Perception, learning, and cognition (p. 643–671). American Psychological Association.

  69. Watanabe S, Huber L (2006) Animal logics: decisions in the absence of human language. Anim Cogn 9:235–245

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

This work was financed by the French Polar Institute (IPEV): project ETHOTAAF 354 to FB and IRFP-NSF (#0700939) Fellowship to APN. We would like to thank Yoanna Marescot for helping with the experiments on the field. We are very grateful to Dora Biro and two anonymous reviewers for their helpful comments on the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Samara Danel.

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.

Video S2. Video of test trial examples in the full information and the exclusion conditions, respectively (MP4 64986 KB)

Table S1. Individuals’ performances (1 successful, 0 unsuccessful) and number of times each subject chose the left or right container in each condition (DOCX 43 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Danel, S., Chiffard-Carricaburu, J., Bonadonna, F. et al. Exclusion in the field: wild brown skuas find hidden food in the absence of visual information. Anim Cogn (2021). https://doi.org/10.1007/s10071-021-01486-4

Download citation

Keywords

  • Avian cognition
  • Charadriiformes
  • Cups task
  • Exclusion performance
  • Inferential reasoning