Avoidance of a moving threat in the common chameleon (Chamaeleo chamaeleon): rapid tracking by body motion and eye use

Abstract

A chameleon (Chamaeleo chamaeleon) on a perch responds to a nearby threat by moving to the side of the perch opposite the threat, while bilaterally compressing its abdomen, thus minimizing its exposure to the threat. If the threat moves, the chameleon pivots around the perch to maintain its hidden position. How precise is the body rotation and what are the patterns of eye movement during avoidance? Just-hatched chameleons, placed on a vertical perch, on the side roughly opposite to a visual threat, adjusted their position to precisely opposite the threat. If the threat were moved on a horizontal arc at angular velocities of up to 85°/s, the chameleons co-rotated smoothly so that (1) the angle of the sagittal plane of the head relative to the threat and (2) the direction of monocular gaze, were positively and significantly correlated with threat angular position. Eye movements were role-dependent: the eye toward which the threat moved maintained a stable gaze on it, while the contralateral eye scanned the surroundings. This is the first description, to our knowledge, of such a response in a non-flying terrestrial vertebrate, and it is discussed in terms of possible underlying control systems.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Angelaki DE, Hess BJM (2005) Self-motion-induced eye movements: effects on visual acuity and navigation. Nat Rev Neurosci 6:966–976. doi:10.1038/nrn1804

    CAS  Article  PubMed  Google Scholar 

  2. Baum T, Katsman I, Rivlin E, Broza M, Moskovitch M, Katzir G (2013) Response of the praying mantis, Sphodromantis viridis, to target change in size and to target visual occlusion. J Insect Behav 27:333–345. doi:10.1007/s10905-013-9422-4

    Article  Google Scholar 

  3. Collett TS (1980) Angular tracking and the optomotor response an analysis of visual reflex interaction in a hoverfly. J Comp Physiol A 140:145–158. doi:10.1007/BF00606306

    Article  Google Scholar 

  4. Collett TS, Land MF (1975) Visual control of flight behaviour in the hoverfly Syritta pipiens L. J Comp Physiol 99:1–66. doi:10.1007/BF01464710

    Article  Google Scholar 

  5. Cronin TW, Nair J, Doyle D (1988) Ocular tracking of rapidly moving visual targets by stomatopod crustaceans. J Exp Biol 138:155–179

    Google Scholar 

  6. Cronin TW, Marshall NJ, Land MF (1991) Optokinesis in gonodactyloid mantis shrimps (Crustacea; Stomatopoda; Gonodactylidae). J Comp Physiol A 168:233–240

    Article  Google Scholar 

  7. Cronin TW, Yan HY, Bidle KAYD (1992) Regional specialization for control of ocular movements in the compound eyes of a stomatopod crustacean. J Exp Biol 393:373–393

    Google Scholar 

  8. Cuadrado M, Martin J, López P (2001) Camouflage and escape decisions in the common chameleon Chamaeleo chamaeleon. Biol J Linn Soc 72:547–554. doi:10.1006/bijl.2000.0515

    Article  Google Scholar 

  9. Feldman JA (1985) Four frames suffice: a provisional model of vision and space. Behav Brain Sci 8:265–289. doi:10.1017/S0140525X00020707

    Article  Google Scholar 

  10. Flanders M (1985) Visually guided head movement in the African chameleon. Vision Res 25:935–942. doi:10.1016/0042-6989(85)90204-4

    CAS  Article  PubMed  Google Scholar 

  11. Flanders M (1988) Head movement co-ordination in the African chameleon. Neuroscience 24:511–517

    CAS  Article  PubMed  Google Scholar 

  12. Fotowat H, Harrison RR, Gabbiani F (2011) Multiplexing of motor information in the discharge of a collision detecting neuron during escape behaviors. Neuron 69:147–158. doi:10.1016/j.neuron.2010.12.007

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Fritsches KA, Marshall J (1999) A new category of eye movements in a small fish. Curr Biol 9:pR272–pR273

    Article  Google Scholar 

  14. Fritsches KA, Marshall NJ (2002) Independent and conjugate eye movements during optokenesis in teleost fish. J Exp Biol 205:1241–1252

    PubMed  Google Scholar 

  15. Harkness L (1977) Chameleons use accommodation cues to judge distance. Nature 267:346–349. doi:10.1038/267346a0

    CAS  Article  PubMed  Google Scholar 

  16. Hassenstein B, Hustert R (1999) Hiding responses of locusts to approaching objects. J Exp Biol 202:1701–1710

    PubMed  Google Scholar 

  17. Heatwole H (1968) Relationship of escape behavior and comuflage in anoline lizards. Copeia 1:109–113

    Article  Google Scholar 

  18. Kelber A, Zeil J (1990) A robust procedure for visual stabilisation of hovering flight position in guard bees of Trigona (Tetragonisca) angustula (Apidae, Meliponinae). J Comp Physiol A 167:569–577. doi:10.1007/BF00190828

    Article  Google Scholar 

  19. Ketter Katz H, Lustig A, Lev-Ari T, Nov Y, Rivlin E, Katzir G (2015) Eye movements in chameleons are not truly independent—evidence from simultaneous monocular tracking of two targets. J Exp Biol 218:2097–2105. doi:10.1242/jeb.113084

    Article  Google Scholar 

  20. Kirmse W, Kirmse R, Milev E (1994) Visuomotor operation in transition from object fixation to prey shooting in chameleons. Biol Cybern 214:209–214

    Article  Google Scholar 

  21. Klier EM, Angelaki DE (2008) Spatial updating and the maintenance of visual constancy. Neuroscience 156:801–818. doi:10.1016/j.neuroscience.2008.07.079

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Land MF (1992) Visual tracking and pursuit: humans and arthropods compared. J Insect Physiol 38:939–951. doi:10.1016/0022-1910(92)90002-U

    Article  Google Scholar 

  23. Land MF (1995) The functions of eye movements in animals remote from man. Stud Vis Inform Proc 6:63–76. doi:10.1016/S0926-907X(05)80006-6

    Article  Google Scholar 

  24. Land MF (2014) Do we have an internal model of the outside world? Philos Trans R Soc B Biol Sci 369:20130045. doi:10.1098/rstb.2013.0045

    Article  Google Scholar 

  25. Land MF (2015) Eye movements of vertebrates and their relation to eye form and function. J Comp Physiol A 201:195–214. doi:10.1007/s00359-014-0964-5

    Article  Google Scholar 

  26. Land MF, Nilsson D-E (2012) Animal eyes, 2nd edn. Oxford University Press, Oxford

    Book  Google Scholar 

  27. Land MF, Marshall JN, Brownless D, Cronin TW (1990) The eye-movements of the mantis shrimp Odontodactylus scyllarus (Crustacea: Stomatopoda). J Comp Physiol A 167:155–166. doi:10.1007/BF00188107

    Article  Google Scholar 

  28. Lustig A, Keter-Katz H, Katzir G (2012a) Threat perception in the chameleon (Chamaeleo chameleon): evidence for lateralized eye use. Anim Cogn 15:609–621. doi:10.1007/s10071-012-0489-7

    Article  PubMed  Google Scholar 

  29. Lustig A, Ketter-Katz H, Katzir G (2012b) Visually guided avoidance in the chameleon (Chamaeleo chameleon): response patterns and lateralization. PLoS One 7:e37875. doi:10.1371/journal.pone.0037875

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Lustig A, Ketter-Katz H, Katzir G (2013a) Lateralization of visually guided detour behaviour in the common chameleon, Chamaeleo chameleon, a reptile with highly independent eye movements. Behav Proc 100:110–115. doi:10.1016/j.beproc.2013.08.002

    Article  Google Scholar 

  31. Lustig A, Ketter-Katz H, Katzir G (2013b) Relating lateralization of eye use to body motion in the avoidance behavior of the chameleon (Chamaeleo chameleon). PLoS One 8:e70761. doi:10.1371/journal.pone.0070761

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Marshall NJ, Land MF, Cronin TW (2014) Shrimps that pay attention: saccadic eye movements in stomatopod crustaceans. Philos Trans R Soc Lond B Biol Sci 369:20130042. doi:10.1098/rstb.2013.0042

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Medan V, Oliva D, Tomsic D (2007) Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus. J Neurophysiol 98:2414–2428. doi:10.1152/jn.00803.2007

    Article  PubMed  Google Scholar 

  34. Mizutani A, Chahl JS, Srinivasan MV (2003) Insect behaviour: motion camouflage in dragonflies. Nature 423:604. doi:10.1038/423604a

    CAS  Article  PubMed  Google Scholar 

  35. Orger MB, Baier H (2005) Channeling of red and green cone inputs to the zebrafish optomotor response. Vis Neurosci 22:275–281. doi:10.1007/3-540-35375-5

    Article  PubMed  Google Scholar 

  36. Ott M (2001) Chameleons have independent eye movements but synchronise both eyes during saccadic prey tracking. Exp Brain Res 139:173–179. doi:10.1007/s002210100774

    CAS  Article  PubMed  Google Scholar 

  37. Ott M, Schaeffel F (1995) A negatively powered lens in the chameleon. Nature 373:692–694

    CAS  Article  PubMed  Google Scholar 

  38. Ott M, Schaeffel F, Kirmse W (1998) Binocular vision and accommodation in prey-catching chameleons. J Comp Physiol A 182:319–330. doi:10.1007/s003590050182

    Article  Google Scholar 

  39. Pettigrew JD, Collin SP, Ott M (1999) Convergence of specialised behaviour, eye movements and visual optics in the sandlance (Teleostei) and the chameleon (Reptilia). Curr Biol 9:421–424. doi:10.1016/S0960-9822(99)80189-4

    CAS  Article  PubMed  Google Scholar 

  40. Sponberg S, Dyhr JP, Hall RW, Daniel TL (2015) Luminance-dependent visual processing enables moth flight in low light. Science 348:1245–1248. doi:10.1126/science.aaa3042

    CAS  Article  PubMed  Google Scholar 

  41. Srinivasan MV, Davey M (1995) Strategies for active camouflage of motion. Proc R Soc B Biol Sci 259:19–25. doi:10.1098/rspb.1995.0004

    Article  Google Scholar 

  42. Taylor EB, McPhail JD (1985) Ontogeny of the startle response in young coho salmon Oncorhynchus kisutch. Trans Am Fish Soc 114:552–557. doi:10.1577/1548-8659(1985)114[552:OOTSRI]2.0.CO;2

    Article  Google Scholar 

  43. Wallman J, Letelier J (1993) Eye movements, head movements, and gaze stabilization in birds. In: Zeigler HP, Bischof HJ (eds) Vision, brain, and behavior in birds. The MIT Press, Cambridge, pp 245–263

    Google Scholar 

  44. Westhoff G, Boetig M, Bleckmann H, Young BA (2010) Target tracking during venom “spitting” by cobras. J Exp Biol 213:1797–1802. doi:10.1242/jeb.037135

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zeil J, Wittmann D (1989) Visually controlled station-keeping by hovering guard bees of Trigona (Tetragonisca) angustula (Apidae, Meliponinae). J Comp Physiol A 165:711–718

    Article  Google Scholar 

Download references

Acknowledgments

The research was supported by the Israel Science Foundation (ISF). We thank Ido Izhaki for statistical advice and Nina Dinov and Nir Keshales for support throughout the research. The thorough comments of the two anonymous referees were of extreme help.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gadi Katzir.

Additional information

T. Lev-Ari and A. Lustig contributed equally to this research.

Electronic supplementary material

Below is the link to the electronic supplementary material.

359_2016_1106_MOESM1_ESM.mpg

Avoidance response of a mature chameleon on a vertical pole to a moving hand (a threat). The chameleon’s abdomen is compressed bilaterally, while the ventrum is directed at the threat. (MPG 4083 kb)

359_2016_1106_MOESM2_ESM.mpg

An overhead view of a just-hatched chameleon on a vertical pole performing an avoidance response. The moving black line provides the direction of the moving threat over the entire angular range. (MPG 5083 kb)

Monocular gaze under three different threat angular velocities. An overhead view of four individuals performing an avoidance response under low (counterclockwise [CCW] and clockwise [CW]), medium (CCW) and high (CW) threat angular velocities. (WMV 13861 kb)

Supplementary Video 1

Avoidance response of a mature chameleon on a vertical pole to a moving hand (a threat). The chameleon’s abdomen is compressed bilaterally, while the ventrum is directed at the threat. (MPG 4083 kb)

Supplementary Video 2

An overhead view of a just-hatched chameleon on a vertical pole performing an avoidance response. The moving black line provides the direction of the moving threat over the entire angular range. (MPG 5083 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lev-Ari, T., Lustig, A., Ketter-Katz, H. et al. Avoidance of a moving threat in the common chameleon (Chamaeleo chamaeleon): rapid tracking by body motion and eye use. J Comp Physiol A 202, 567–576 (2016). https://doi.org/10.1007/s00359-016-1106-z

Download citation

Keywords

  • Visually guided tracking
  • Threat avoidance
  • Eye movement
  • Chameleon
  • Role-dependent eye movement