Threat perception in the chameleon (Chamaeleo chameleon): evidence for lateralized eye use

Abstract

Chameleons are arboreal lizards with highly independent, large amplitude eye movements. In response to an approaching threat, a chameleon on a vertical pole moves so as to keep itself away from the threat. In so doing, it shifts between monocular and binocular scanning of the threat and of the environment. We analyzed eye movements in the Common chameleon, Chamaeleo chameleon, during avoidance response for lateralization, that is, asymmetry at the functional/behavioral levels. The chameleons were exposed to a threat, approaching horizontally from clockwise or anti-clockwise directions, and that could be viewed monocularly or binocularly. Our results show three broad patterns of eye use, as determined by durations spent viewing the threat and by frequency of eye shifts. Under binocular viewing, two of the patterns were found to be both side dependent, that is, lateralized and role dependent ("leading" or "following"). However, under monocular viewing, no such lateralization was detected. We discuss these findings in light of the situation not uncommon in vertebrates, of independent eye movements and a high degree of optic nerve decussation and that lateralization may well occur in organisms that are regularly exposed to critical stimuli from all spatial directions. We point to the need of further investigating lateralization at fine behavioral levels.

Lateralization of Eye Use in Cuttlefish: Opposite Direction for Anti-Predatory and Predatory Behaviors

“…Vertebrates with laterally placed eyes typically show preferential eye use for ecological activities including scanning for potential predators (Franklin and Lima, 2001; Koboroff et al, 2008; Lustig et al, 2010; Martin et al, 2010) or searching for prey (Mench and Andrew, 1983; Robins and Rogers, 2004; Ventolini et al, 2005; Bonati et al, 2008). Processing visual information predominately through the left or right visual field has been associated with specialized function of the left and right brain (i.e., lateralized brain function; Rogers et al, 2013).…”

Relating Lateralization of Eye Use to Body Motion in the Avoidance Behavior of the Chameleon (Chamaeleo chameleon)

“…A further analysis revealed two similar-sized sub-groups in terms of body motion [34]: One exhibited significantly lower exposure (and thus better concealment) to a threat approaching from the right (termed “right-biased sub-group”) and the other – to a threat approaching from the left (termed “left-biased sub-group”). This lateralization of body exposure was observed under conditions that allowed only monocular or both monocular and binocular viewing of the threat [33], [34].…”

“…Collection, maintenance and experimentation with the experimental animals (common chameleons, Chamaeleo chameleon ) were performed under permits from the Israeli Nature and Parks Authority (permit 2011/11411) and were specifically approved by the University of Haifa ethics committee (permit 095/08). Methods are provided here in brief; further details can be found elsewhere [33].…”

“…We previously demonstrated that during avoidance, eye use [33] is lateralized under binocular but not under monocular viewing of the threat. Also, the patterns of body motion and thus of body exposure, were lateralized at the tested group level (N = 26).…”

“…While their movements are typically slow, chameleons perform rapid and highly precise body-position corrections while avoiding a threat [33], [34]. Upon the approach of a threat (e.g., a predator or a human), a chameleon will change its position on a perch so as to keep its body on the side of the perch distal to the threat, thus, minimizing its body exposure.…”