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A review of visual perception mechanisms that regulate rapid adaptive camouflage in cuttlefish

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Abstract

We review recent research on the visual mechanisms of rapid adaptive camouflage in cuttlefish. These neurophysiologically complex marine invertebrates can camouflage themselves against almost any background, yet their ability to quickly (0.5–2 s) alter their body patterns on different visual backgrounds poses a vexing challenge: how to pick the correct body pattern amongst their repertoire. The ability of cuttlefish to change appropriately requires a visual system that can rapidly assess complex visual scenes and produce the motor responses—the neurally controlled body patterns—that achieve camouflage. Using specifically designed visual backgrounds and assessing the corresponding body patterns quantitatively, we and others have uncovered several aspects of scene variation that are important in regulating cuttlefish patterning responses. These include spatial scale of background pattern, background intensity, background contrast, object edge properties, object contrast polarity, object depth, and the presence of 3D objects. Moreover, arm postures and skin papillae are also regulated visually for additional aspects of concealment. By integrating these visual cues, cuttlefish are able to rapidly select appropriate body patterns for concealment throughout diverse natural environments. This sensorimotor approach of studying cuttlefish camouflage thus provides unique insights into the mechanisms of visual perception in an invertebrate image-forming eye.

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References

  • Allen JJ, Mäthger LM, Barbosa A, Hanlon RT (2009) Cuttlefish use visual cues to control three-dimensional skin papillae for camouflage. J Comp Physiol A 195:547–555

    Article  Google Scholar 

  • Allen JJ, Mäthger LM, Barbosa A, Buresch KC, Sogin E, Schwartz J, Chubb C, Hanlon RT (2010) Cuttlefish dynamic camouflage: responses to substrate choice and integration of multiple visual cues. Proc Biol Sci 277:1031–1039

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson JC, Baddeley RJ, Osorio D, Shashar N, Tyler CW, Ramachandran VS, Crook AC, Hanlon RT (2003) Modular organization of adaptive colouration in flounder and cuttlefish revealed by independent component analysis. Network 14:321–333

    Article  CAS  PubMed  Google Scholar 

  • Barbosa A, Mäthger LM, Chubb C, Florio C, Chiao C-C, Hanlon RT (2007) Disruptive coloration in cuttlefish: a visual perception mechanism that regulates ontogenetic adjustment of skin patterning. J Exp Biol 210:1139–1147

    Article  PubMed  Google Scholar 

  • Barbosa A, Litman L, Hanlon RT (2008a) Changeable cuttlefish camouflage is influenced by horizontal and vertical aspects of the visual background. J Comp Physiol A 194:405–413

    Article  Google Scholar 

  • Barbosa A, Mäthger LM, Buresch KC, Kelly J, Chubb C, Chiao C-C, Hanlon RT (2008b) Cuttlefish camouflage: The effects of substrate contrast and size in evoking uniform, mottle or disruptive body patterns. Vision Res 48:1242–1253

    Article  PubMed  Google Scholar 

  • Barbosa A, Allen JJ, Mäthger LM, Hanlon RT (2012) Cuttlefish use visual cues to determine arm postures for camouflage. Proc Biol Sci 279:84–90

    Article  PubMed Central  PubMed  Google Scholar 

  • Bex PJ, Makous W (2002) Spatial frequency, phase, and the contrast of natural images. J Opt Soc Am A: 19:1096–1106

    Article  Google Scholar 

  • Boycott BB (1961) The functional organization of the brain of the cuttlefish Sepia officinalis. Proc R Soc Lond B 153:503–534

    Article  Google Scholar 

  • Buresch KC, Mathger LM, Allen JJ, Bennice C, Smith N, Schram J, Chiao C-C, Chubb C, Hanlon RT (2011) The use of background matching vs. masquerade for camouflage in cuttlefish Sepia officinalis. Vision Res 51:2362–2368

    Article  PubMed  Google Scholar 

  • Chiao C-C, Hanlon RT (2001a) 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 

  • Chiao C-C, Hanlon RT (2001b) Cuttlefish cue visually on area - not shape or aspect ratio - of light objects in the substrate to produce disruptive body patterns for camouflage. Biol Bull 201:269–270

    Article  CAS  PubMed  Google Scholar 

  • Chiao C-C, Kelman EJ, Hanlon RT (2005) Disruptive body patterning of cuttlefish (Sepia officinalis) requires visual information regarding edges and contrast of objects in natural substrate backgrounds. Biol Bull 208:7–11

    Article  PubMed  Google Scholar 

  • Chiao C-C, Chubb C, Hanlon RT (2007) Interactive effects of size, contrast, intensity and configuration of background objects in evoking disruptive camouflage in cuttlefish. Vision Res 47:2223–2235

    Article  PubMed  Google Scholar 

  • Chiao C-C, Chubb C, Buresch K, Siemann L, Hanlon RT (2009) The scaling effects of substrate texture on camouflage patterning in cuttlefish. Vision Res 49:1647–1656

    Article  PubMed  Google Scholar 

  • Chiao C-C, Chubb C, Buresch KC, Barbosa A, Allen JJ, Mäthger LM, Hanlon RT (2010) Mottle camouflage patterns in cuttlefish: quantitative characterization and visual background stimuli that evoke them. J Exp Biol 213:187–199

    Article  PubMed  Google Scholar 

  • Chiao C-C, Ulmer KM, Siemann LA, Buresch KC, Chubb C, Hanlon RT (2013) How visual edge features influence cuttlefish camouflage patterning. Vision Res 83:40–47

    Article  PubMed  Google Scholar 

  • Chichery R, Chanelet J (1976) Motor and behavioral responses obtained by stimulation with chronic electrodes of the optic lobe of Sepia officinalis. Brain Res 105:525–532

    Article  CAS  PubMed  Google Scholar 

  • Chung WS, Marshall NJ (2014) Range-finding in squid using retinal deformation and image blur. Curr Biol 24:R64–R65

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Bellido PT, Wardill TJ, Buresch KC, Ulmer KM, Hanlon RT (2014) Expression of squid iridescence depends on environmental luminance and peripheral ganglion control. J Exp Biol 217:850–858

    Article  CAS  PubMed  Google Scholar 

  • Hanlon RH (2007) Cephalopod dynamic camouflage. Curr Biol 17:R400–R404

    Article  CAS  PubMed  Google Scholar 

  • Hanlon RT, Messenger JB (1988) Adaptive coloration in young cuttlefish (Sepia officinalis L.): The morphology and development of body patterns and their relation to behaviour. Philos Trans R Soc Lond B 320:437–487

    Article  Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod Behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Hanlon RT, Chiao C-C, Mäthger LM, Barbosa A, Buresch KC, Chubb C (2009) Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philos Trans R Soc Lond B Biol Sci 364:429–437

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanlon RT, Chiao C-C, Mäthger LM, Buresch KC, Barbosa A, Allen JJ, Siemann L, Chubb C (2011) Rapid adaptive camouflage in cephalopods. In: Stevens M, Merilaita S (eds) Animal camouflage: mechanisms and functions. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

  • Hanlon RT, Chiao C-C, Mathger LM, Marshall NJ (2013) A fish-eye view of cuttlefish camouflage using in situ spectrometry. Biol J Linn Soc 109:535–551

    Article  Google Scholar 

  • Kelman EJ, Tiptus P, Osorio D (2006) Juvenile plaice (Pleuronectes platessa) produce camouflage by flexibly combining two separate patterns. J Exp Biol 209:3288–3292

    Article  PubMed  Google Scholar 

  • Kelman EJ, Baddeley RJ, Shohet AJ, Osorio D (2007) Perception of visual texture and the expression of disruptive camouflage by the cuttlefish, Sepia officinalis. Proc Biol Sci 274:1369–1375

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kelman EJ, Osorio D, Baddeley RJ (2008) A review of cuttlefish camouflage and object recognition and evidence for depth perception. J Exp Biol 211:1163–1757

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Mäthger LM, Chiao C-C, Barbosa A, Buresch KC, Kaye S, Hanlon RT (2007) Disruptive coloration elicited on controlled natural substrates in cuttlefish, Sepia officinalis. J Exp Biol 210:2657–2666

    Article  PubMed  Google Scholar 

  • Mäthger LM, Roberts SB, Hanlon RT (2010) Evidence for distributed light sensing in the skin of cuttlefish, Sepia officinalis. Biol Lett 6:600–603

    Article  PubMed Central  PubMed  Google Scholar 

  • Mäthger LM, Hanlon RT, Hakansson J, Nilsson DE (2013) The W-shaped pupil in cuttlefish (Sepia officinalis): functions for improving horizontal vision. Vision Res 83:19–24. doi:10.1016/j.visres.2013.02.016

    Article  PubMed  Google Scholar 

  • Messenger JB (1991) Photoreception and vision in molluscs. In: Cronly-Dillon JR, Gregory RL (eds) Vision and visual dysfunction, vol 2., Evolution of the eye and visual systemMacmillan Press, London, pp 364–397

    Google Scholar 

  • Messenger JB (2001) Cephalopod chromatophores: Neurobiology and natural history. Biol Rev 76:473–528

    Article  CAS  PubMed  Google Scholar 

  • Nilsson DE, Warrant EJ, Johnsen S, Hanlon RT, Shashar N (2013) The giant eyes of giant squid are indeed unexpectedly large, but not if used for spotting sperm whales. BMC Evol Biol 13:187

    Article  PubMed Central  PubMed  Google Scholar 

  • Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev 47:241–307

    Article  CAS  Google Scholar 

  • Packard A (1982) Morphogenesis of chromatophore patterns in cephalopods: Are morphological and physiological ‘units’ the same? Malacologia 23:193–201

    Google Scholar 

  • Ramachandran VS, Tyler CW, Gregory RL, Rogers-Ramachandran D, Duensing S, Pillsbury C, Ramachandran C (1996) Rapid adaptive camouflage in tropical flounders. Nature 379(6568):815–818

    Article  CAS  PubMed  Google Scholar 

  • Saidel WM (1988) How to be unseen: An essay in obscurity. In: Fay RR, Popper AN, Tavolga WN (eds) Atema J. Sensory Biology of Aquatic Animals Springer-Verlag, New York, pp 487–513

    Google Scholar 

  • Shohet A, Baddeley R, Anderson J, Osorio D (2007) Cuttlefish camouflage: a quantitative study of patterning. Biol J Linn Soc 92:335–345

    Article  Google Scholar 

  • Stevens M, Merilaita S (2011) Animal Camouflage: Mechanisms and Function. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Troscianko T, Benton CP, Lovell PG, Tolhurst DJ, Pizlo Z (2009) Camouflage and visual perception. Philos Trans R Soc Lond B 364:449–461

    Article  Google Scholar 

  • Tublitz NJ, Gaston MR, Loi PK (2006) Neural regulation of a complex behavior: body patterning in cephalopod molluscs. Integr Comp Biol 46:880–889

    Article  CAS  PubMed  Google Scholar 

  • Tyrie EK, Hanlon RT, Siemann L, Uyarra MC (2015) Coral reef flounders, Bothus lunatus, choose substrates on which they can achieve camouflage with their limited body pattern repertoire. Biol J Linn Soc (in press)

  • Young JZ (1962) The optic lobes of Octopus vulgaris. Philos Trans R Soc Lond B 245:19–58

    Article  Google Scholar 

  • Young JZ (1974) The central nervous system of Loligo. I. The optic lobe. Philos Trans R Soc Lond B 267:263–302

    Article  CAS  Google Scholar 

  • Zylinski S, Osorio D (2011) What can camouflage tell us about non-human visual perception? A case study of multiple cue use in the cuttlefish. In: Stevens M, Merilaita S (eds) Animal camouflage: mechanisms and functions. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

  • Zylinski S, Osorio D, Shohet AJ (2009a) Edge detection and texture classification by cuttlefish. J Vision 9:1–10

    Article  Google Scholar 

  • Zylinski S, Osorio D, Shohet AJ (2009b) Perception of edges and visual texture in the camouflage of the common cuttlefish, Sepia officinalis. Philos Trans R Soc Lond B 364:439–448

    Article  CAS  Google Scholar 

  • Zylinski S, Darmaillacq AS, Shashar N (2012) Visual interpolation for contour completion by the European cuttlefish (Sepia officinalis) and its use in dynamic camouflage. Proc Biol Sci 279:2386–2390

    Article  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Program in Sensory Physiology and Behavior, Marine Biological Laboratory, Woods Hole, MA, USA

    Chuan-Chin Chiao, Charles Chubb & Roger T. Hanlon

  2. Department of Life Science and Institute of Systems Neuroscience, National Tsing Hua University, 101, Sec 2, Kuang-Fu Road, Hsinchu, 30013, Taiwan

    Chuan-Chin Chiao

  3. Department of Cognitive Sciences and Institute for Mathematical Behavioral Sciences, University of California at Irvine, Irvine, USA

    Charles Chubb

  4. Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA

    Roger T. Hanlon

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  1. Chuan-Chin Chiao
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Correspondence to Chuan-Chin Chiao.

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Chiao, CC., Chubb, C. & Hanlon, R.T. A review of visual perception mechanisms that regulate rapid adaptive camouflage in cuttlefish. J Comp Physiol A 201, 933–945 (2015). https://doi.org/10.1007/s00359-015-0988-5

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