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Cuttlefish perform multiple agonistic displays to communicate a hierarchy of threats

Abstract

Many animals produce multiple displays during agonistic interactions, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis has been proposed to explain their occurrence and posits that different displays convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. This hypothesis suggests that low-risk signals, typically performed at the beginning stages of an interaction, are strong predictors of high-risk signals but weak predictors of physical aggression. High-risk signals, typically produced at later stages of an interaction, are strong predictors of physical aggression. We used giant Australian cuttlefish, Sepia apama, to test these predictions. We combined field observations and laboratory video playback experiments to determine whether (i) male cuttlefish produce specific sequences of displays, (ii) displays in early stages of an interaction predict displays in later stages of an interaction, and (iii) displays produced in later stages of an interaction provide reliable predictors of physical aggression. Field observations suggested that males progressed from low-risk to high-risk signals (i.e., visual signaling to physical aggression). Video playback results zrevealed that the low-risk frontal display, produced during early stages of an interaction, conveys reliable information about the cuttlefish’s intent to escalate to later stages of visual signaling. Both the shovel and lateral displays were produced during the later stages of signaling and were reliable predictors of subsequent physical aggression. Our study supports the hierarchical signaling hypothesis and provides new empirical insights into how cuttlefish use progressive visual signaling to convey increasing levels of threat.

Significance statement

Many animals perform multiple displays during fights, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis posits that animals produce multiple displays to convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. We tested this hypothesis in giant Australian cuttlefish, Sepia apama. Specifically, we tested whether (i) displays in early stages of a fight predict displays in later stages of a fight and (ii) displays produced in later stages of a fight provide reliable predictors of physical aggression. Our results support these predictions and reveal that fighting cuttlefish progress from low-risk signals to high-risk signals to convey a hierarchy of threats. This study highlights the generality of hierarchical signaling during animal contests, as cuttlefish are evolutionary far removed from many of the species that have been reported to use this type of signaling.

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References

  1. Adamo SA, Hanlon RT (1996) Do cuttlefish (Cephalopoda) signal their intentions to conspecifics during agonistic encounters? Anim Behav 52:73–81

    Article  Google Scholar 

  2. Adams ES, Mesterton-Gibbons M (1995) The cost of threat displays and the stability of deceptive communication. J Theor Biol 175:405–421

    Article  Google Scholar 

  3. Akçay Ç, Tom ME, Campbell SE, Beecher MD (2013) Song type matching is an honest threat signal in a hierarchical animal communication system. Proc R Soc Lond B 280:20122512

    Article  Google Scholar 

  4. Andersson M (1980) Why are there so many threat displays? J Theor Biol 86:773–781

    CAS  Article  PubMed  Google Scholar 

  5. ASAB/ABS (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309

    Article  Google Scholar 

  6. Ballentine B, Searcy WA, Nowicki S (2008) Reliable aggressive signalling in swamp sparrows. Anim Behav 75:693–703

    Article  Google Scholar 

  7. Bartos L, Fricova B, Bartosova-Vichova J, Panama J, Sustr P, Smidova E (2007) Estimation of the probability of fighting in fallow deer (Dama dama) during the rut. Aggress Behav 33:7–13

    Article  PubMed  Google Scholar 

  8. Bellingham J, Morris AG, Hunt DM (1998) The rhodopsin gene of the cuttlefish Sepia officinalis: sequence and spectral tuning. J Exp Biol 201:2299–2306

    CAS  PubMed  Google Scholar 

  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 57:289–300

    Google Scholar 

  10. Blumstein D, Evans CS, Daniel JC (2006) JWatcher 1.0. http://www.jwatcher.ucla.edu/

  11. Boal JG, Shashar N, Grable MM, Vaughan KH, Loew ER, Hanlon RT (2004) Behavioral evidence for intraspecific signals with achromatic and polarized light by cuttlefish (Mollusca: Cephalopoda). Behaviour 141:837–861

    Article  Google Scholar 

  12. Brown PK, Brown PS (1958) Visual pigments of octopus and cuttlefish. Nature 182:1288–1290

    CAS  Article  PubMed  Google Scholar 

  13. Chiao CC, Hanlon RT (2001) Cuttlefish camouflage: visual perception of size, contrast and number of white squares on artificial checkerboard substrata initiates disruptive coloration. J Exp Biol 204:2119–2125

    CAS  PubMed  Google Scholar 

  14. Chiou TH, Mäthger LM, Hanlon RT, Cronin TW (2007) Spectral and spatial properties of polarized light reflections from the arms of squid (Loligo pealeii) and cuttlefish (Sepia officinalis L.). J Exp Biol 210:3624–3635

    Article  PubMed  Google Scholar 

  15. Clutton-Brock TH, Albon SD (1979) The roaring of red deer and the evolution of honest advertisement. Behaviour 69:145–170

    Article  Google Scholar 

  16. Clutton-Brock TH, Huchard E (2013) Social competition and selection in males and females. Proc R Soc Lond B 268:20130074

    Google Scholar 

  17. Decourcy KR, Jenssen TA (1994) Structure and use of male territorial headbob signals by the lizard Anolis carolinensis. Anim Behav 47:251–262

    Article  Google Scholar 

  18. DiMarco FP, Hanlon RT (1997) Agonistic behavior in the squid Loligo plei (Loliginidae Teuthoidea): fighting tactics and the effects of size and resource value. Ethology 103:89–108

    Article  Google Scholar 

  19. Egge AR, Brandt Y, Swallow JG (2011) Sequential analysis of aggressive interactions in the stalk-eyed fly Teleopsis dalmanni. Behav Ecol Sociobiol 65:369–379

    Article  Google Scholar 

  20. Enquist M (1985) Communication during aggressive interactions with particular reference to variation in choice of behaviour. Anim Behav 33:1152–1161

    Article  Google Scholar 

  21. Evans CS, Marler P (1991) On the use of video images as social stimuli in birds: audience effects on alarm calling. Anim Behav 41:17–26

    Article  Google Scholar 

  22. Fischer J, Kitchen D, Seyfarth R, Cheney D (2004) Baboon loud calls advertise male quality: acoustic features and their relation to rank, age, and exhaustion. Behav Ecol Sociobiol 56:140–148

    Article  Google Scholar 

  23. Hall KC, Hanlon RT (2002) Principal features of the mating system of a large aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545

    Article  Google Scholar 

  24. Hamasaki DI (1968) The electroretinogram of the intact anesthetized octopus. Vis Res 8:247–258

    CAS  Article  PubMed  Google Scholar 

  25. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge, MA

    Google Scholar 

  26. Hanlon RT, Naud MJ, Shaw PW, Havenhand JN (2005) Transient sexual mimicry leads to fertilization. Nature 433:212

    CAS  Article  PubMed  Google Scholar 

  27. Hazlett BA, Bossert WH (1965) A statistical analysis of the aggressive communication systems of some hermit crabs. Anim Behav 13:357–373

    CAS  Article  PubMed  Google Scholar 

  28. Hemmi JM, Zeil J (2003) Burrow surveillance in fiddler crabs. I. Description of behaviour. J Exp Biol 206:3935–3950

    Article  PubMed  Google Scholar 

  29. Hinde RA (1981) Animal signals: ethological and games-theory approaches are not incompatible. Anim Behav 29:535–542

    Article  Google Scholar 

  30. Hof D, Hazlett N (2010) Low-amplitude song predicts attack in a North American wood warbler. Anim Behav 80:821–828

    Article  Google Scholar 

  31. Hof D, Podos J (2013) Escalation of aggressive vocal signals: a sequential playback study. Proc R Soc Lond B 280:20131553

    Article  Google Scholar 

  32. Johnstone RA (2001) EavesdropPing and animal conflict. Proc Natl Acad Sci U S A 90:9177–9180

    Article  Google Scholar 

  33. Johnstone RA, Bshary R (2004) Evolution of spite through indirect reciprocity. Proc R Soc Lond B 271:1917–1922

    Article  Google Scholar 

  34. Johnstone RA, Grafen A (1993) Dishonesty and the handicap principle. Anim Behav 46:759–764

    Article  Google Scholar 

  35. Kitchen D, Seyfarth R, Fischer J, Cheney D (2003) Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:374–384

    Google Scholar 

  36. Kokko H (1997) Evolutionarily stable strategies of age-dependent sexual advertisement. Behav Ecol Sociobiol 41:99–107

    Article  Google Scholar 

  37. Lange H, Leimar O (2003) The function of threat display in wintering great tits. Anim Behav 64:573–584

    Article  Google Scholar 

  38. Marshall NJ, Messenger JB (1996) Colour-blind camouflage. Nature 382:408–409

    CAS  Article  Google Scholar 

  39. Mäthger LM, Barbosa A, Miner S, Hanlon RT (2006) Color blindness and contrast perception in cuttlefish (Sepia officinalis) determine by a visual sensorimotor assay. Vis Res 46:1746–1753

    Article  PubMed  Google Scholar 

  40. Mäthger LM, Shashar N, Hanlon RT (2009) Do cephalopods communicate using polarized light reflections from their skin? J Exp Biol 212:2133–2140

    Article  PubMed  Google Scholar 

  41. Maynard Smith J (1974) The theory of games and the evolution of animal conflicts. J Theor Biol 47:209–221

    Article  Google Scholar 

  42. Maynard Smith J (1982) The evolution and the theory of games. Cambridge University Press, London

    Book  Google Scholar 

  43. Maynard Smith J, Price GR (1973) The logic of animal conflict. Nature 246:15–18

    Article  Google Scholar 

  44. McGregor PK (1993) Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Philos Trans R Soc Lond B 340:237–244

    Article  Google Scholar 

  45. Mouterde SC, Duganzich DM, Molles LE, Helps S, Helps F, Waas JR (2012) Triumph displays inform eavesdropping little blue penguins of new dominance asymmetries. Anim Behav 83:605–611

    Article  Google Scholar 

  46. Moynihan M (1985) Communication and noncommunication by cephalopods. Indiana University Press, Bloomington, IL

    Google Scholar 

  47. NHMRC (National Health and Medical Research Council), (2004) Australian code of practice for the care and use of animals for scientific purposes. 7th edition. http://www.bhmrc.gov.au/publications/synopses/ea16syn.htm

  48. Parker GA (1974) Assessment strategy and evolution of fighting behaviour. J Theor Biol 47:223–243

    CAS  Article  PubMed  Google Scholar 

  49. Peake TM (2005) Eavesdropping in communication networks. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp. 13–37

    Chapter  Google Scholar 

  50. Popp JW (1987a) Risk and effectiveness in the use of agonistic displays by American goldfinches. Behaviour 103:141–156

    Article  Google Scholar 

  51. Popp JW (1987b) Agonistic communication among wintering purple finches. Wilson Bull 99:97–100

    Google Scholar 

  52. Povinelli DJ, Gallup GGJ, Eddy TJ, Bierschwale DT, Engstrom MC, Perilloux HK, Toxopeus IB (1997) Chimpanzees recognize themselves in mirrors. Anim Behav 53:1083–1088

    Article  Google Scholar 

  53. Poynton C (2003) Digital video and HDTV: algorithms and interfaces. Morgan Kaufmann Publishers, San Francisco

    Google Scholar 

  54. Pronk R, Wilson DR, Harcourt R (2010) Video playback demonstrates episodic personality in the gloomy octopus. J Exp Biol 213:1035–1042

    CAS  Article  PubMed  Google Scholar 

  55. Rosenthal GG, Evans CS, Miller WL (1996) Female preference for dynamic traits in the green swordtail, Xiphophorus helleri. Anim Behav 51:811–820

    Article  Google Scholar 

  56. Rowell J, Ellner SP, Reeve HK (2006) Why animals lies: how dishonesty and belief can coexist in a signaling system. Am Nat 168:E180–E204

    Article  PubMed  Google Scholar 

  57. Rowland WJ (2000) Habituation and development of response specificity to a sign stimulus: male preference for female courtship posture in stickleback. Anim Behav 60:63–68

    Article  PubMed  Google Scholar 

  58. Schnell AK, Smith CL, Hanlon RT, Harcourt R (2015) Giant Australian cuttlefish use mutual assessment to resolve male-male contests. Anim Behav 107:31–40

    Article  Google Scholar 

  59. Searcy WA, Beecher MD (2009) Song as an aggressive signal in songbirds. Anim Behav 78:128–1292

    Article  Google Scholar 

  60. Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton, NJ

    Google Scholar 

  61. Searcy WA, DuBois AL, Rivera-Cáceres K, Nowicki S (2013) A test of a hierarchical signalling in song sparrows. Anim Behav 86:309–315

    Article  Google Scholar 

  62. Shashar N, Rutledge PS, Cronin TW (1996) Polarization vision in cuttlefish—a concealed communication channel? J Exp Biol 199:2077–2084

    PubMed  Google Scholar 

  63. Shashar N, Milbury CA, Hanlon RT (2002) Polarization vision in cephalopods: neuroanatomical and behavioral features that illustrate aspects of form and function. Mar Freshwater Behav Physiol 35:57–68

    Article  Google Scholar 

  64. Számadó S (2000) Cheating as a mixed strategy in a simple model of aggressive communication. Anim Behav 59:221–230

  65. Talbot CM, Marshall J (2010) Polarization sensitivity in two species of cuttlefish—Sepia plangon (Gray 1849) and Sepia mestus (Gray 1849)—demonstrated with polarized optomotor stimuli. J Exp Biol 213:3364–3370

    Article  PubMed  Google Scholar 

  66. Talbot CM, Marshall JN (2011) The retinal topography of three species of coleoid cephalopod: significance for perception of polarized light. Philos Trans R Soc Lond B 366:724–733

    Article  Google Scholar 

  67. van Rhijn JG, Vodegel R (1980) Being honest about one’s intentions: an evolutionary stable strategy for animal conflicts. J Theor Biol 85:623–641

    Article  PubMed  Google Scholar 

  68. van Staaden MJ, Searcy WA, Hanlon RT (2011) Signalling aggression. In: Huber R, DL B, Brennan P (eds) Aggression. Elsevier Academic Press, San xDiego, CA, pp. 23–49

  69. Vehrencamp SL, Hall ML, Bohman ER, Depeine CD, Dalziel AH (2007) Song matching, overlapping, and switching in the banded wren: the sender’s perspective. Behav Ecol 18:849–859

    Article  PubMed  PubMed Central  Google Scholar 

  70. Verhoeven KJF, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Article  Google Scholar 

  71. Waas JR (1991a) The risks and benefits of signalling aggressive motivation: a study of cave-dwelling little blue penguins. Behav Ecol Sociobiol 29:139–146

    Article  Google Scholar 

  72. Waas JR (1991b) Do little penguins signal their intentions during aggressive interactions with strangers? Anim Behav 41:375–382

    Article  Google Scholar 

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Acknowledgments

In South Australia, we thank T. Bramley of Whyalla Diving Services and the Sholley Foundation. In NSW, we thank S. Baxter and P. Simpson for the field assistance, J. Lustosa for the assistance with behavioral scoring, D. Barker of Cronulla Fisheries Research Centre for the aquaria maintenance and animal husbandry, and the Cronulla Fisheries Research Centre for the use of their facilities.

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Correspondence to Alexandra K. Schnell.

Ethics declarations

All applicable international, national, and/or institutional guidelines for care and use of animals were followed. Subject collection was approved under a NSW Industry & Investment Permit Reference number: P08/0039-3. This research conformed to the Guidelines for the Treatment of Animals in Behavioural Research and Teaching (ASAB/ABS 2012) and was completed in compliance with the Australian Code of Practice for the Care and Use of Animals for Scientific Purpose (NHMRC 2004). All procedures were approved under Macquarie University AEC Reference number: 2010/029 and Department of Primary Industries ACEC Reference number: 12/04. This article does not contain any studies with human participants performed by any of the authors.

Funding

This study was funded by the Macquarie University Excellence Scholarship awarded to A. K. Schnell (grant number not available).

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The authors declare that they have no competing interests.

Additional information

Communicated by S. Sakaluk

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Schnell, A.K., Smith, C.L., Hanlon, R.T. et al. Cuttlefish perform multiple agonistic displays to communicate a hierarchy of threats. Behav Ecol Sociobiol 70, 1643–1655 (2016). https://doi.org/10.1007/s00265-016-2170-7

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Keywords

  • Reliable signals
  • Graded aggression
  • Visual communication
  • Cephalopod
  • Hierarchical signaling hypothesis
  • Video playback