Non–mammals (NM, ectotherms & birds) differ from mammals in important aspects that determine what sections of space are sampled and how visual information is acquired. Unlike mammals, many NM show independent eye movements and high levels of optic nerve decussation. Consequently, studies of visual processes in NM should not be constrained by “mammalian / primate models”.

We studied eye use during visually guided behaviour in chameleons (Chamaeleo chameleon; Chamaeleonidae; Reptilia), as a NM model. In scanning the environment, chameleons perform large-amplitude eye movements, referred to as “independent”. When prey (insect) is detected, the eyes converge binocularly, “lock” in their sockets and visual tracking is by head movements. We asked: (i) How independent are eye movements? (ii) How related are movements to context?

Chameleons, presented with two small targets, moving in opposite directions, performed synchronous, smooth, monocular tracking. Similar to primate smooth pursuits and saccades, tracking here comprised alternating “smooth” phases and abrupt “steps”, that differed between monocular and binocular states. In avoiding a moving threat, the chameleons performed a highly precise, smooth counter-rotation of the body on the perch (gain = 1) achieving maximal concealment. Eye use during rotation was context dependent, with one eye fixating the threat and the other –scanning independently.

We propose that eye movements in chameleons are not simply “independent”. Rather, they are (i) independent during scanning, (ii) conjugate during binocular tracking of small targets and (iii) disconjugate, yet coordinated, during monocular tracking. These results support the view that basic monocular control is under higher levels of regulation that dictate the eyes' level of coordination according to context. These novel findings are discussed in relation to NM vision.