Conjugate and Disjunctive Saccades in Contrasting Oculomotor Strategies’ Two Avian Species with

We have recorded with the magnetic search coil method the spontaneous saccades of two species of predatory birds, which differ in the relative importance of panoramic and fovea1 vision. The little eagle (Haliaetus morphnoides) hunts from great heights and has no predators, whereas the tawny frogmouth (Podargus strigoides) hunts from perches near the ground, is preyed upon, and frequently adopts an immobile camouflage posture. We find that both birds spend most of the time with their eyes confined to a small region of gaze, the primary position of gaze; in this position, the visual axes are much more diverged in the frogmouth than in the eagle, thereby giving it a larger total field of view at the expense of its binocular field. Both species, however, can align their visual axes, thereby gaining a binocular view of targets in the frontal visual field. The eagle makes saccades 10 times as frequently as the frogmouth, and in most of its saccades the eyes move in the same direction, although the eye movements are generally not conjugate; in most frogmouth saccades, on the other hand, the eyes move in opposite directions. We discuss these phenomena in terms of their saccadic mechanisms and their possible adaptiveness. We also report two incidental observations: in certain circumstances, the frogmouth shows no sign of having a vestibulo-ocular reflex, and the eagle, although the quintessential foveate animal, shows extreme directional asymmetries of monocularly evoked optokinetic nystagmus. Although much is known about the mechanism of production of saccadic eye movements and of the details of saccadic trajectories, little is known about what determines the timing, direction, and amplitudes of saccades produced in normal life. One possibility is that all of the thousands of saccades made daily are directed at particular targets. Alternatively, it may be that in the absence of specific targets, saccades are made nonetheless with some statistically definable pattern of directions, amplitudes, and intersaccadic Recerved July 13, 1984; Revised December 18, 1984 Accepted January 2, 1985 ’ This work was supported by National institutes of Health Grant EY02937 to J. W. and grants from the Australian National Health and Medical Research Council to J. D. P. ‘To whom correspondence should be addressed, at Department of Biology, City College of City University of New York, Convent Avenue and 138th Street, New York, NY 10031. 3 Present address: Department of Physiology, University of Queensland, St. Lucia, QLD 4067, Australia. intervals. We hypothesize that saccades have such an endogenous pattern in time and space, and that this pattern represents an oculomotor strategy for a species. As a start in investigating this hypothesis, we have taken advantage of the diversity of avian visual adaptations by studying spontaneous saccades made by two species, the tawny frogmouth and the little eagle, which we presume have different oculomotor requirements, particularly with respect to binocular coordination. The saccades of both eyes were studied as the animals freely viewed the laboratory with their heads restrained. Although this situation is of course far from what the animals would experience in their natural circumstances, it provides an opportunity to compare the two species under identical conditions without the complication of differences in head movements. To aid in the interpretation of differences in oculomotor behavior in the two species, we will briefly describe their natural history. The tawny frogmouth (Podargus strigoides) is a representative of a Gondwanaland group of Caprimulgiformes, which are close relatives of the owls (Fig. 1). The following account of their habits is taken from Schodde and Mason (1981). Like owls, the frogmouth is a nocturnal predator, feeding on invertebrates and small vertebrates which it takes mostly on the ground after short sallies from a low perch, although a small amount of aerial feeding also occurs. As a camouflage strategy, the frogmouth relies heavily on its cryptic plumage and a posture in which it resembles a broken branch. This camouflage strategy is sufficiently effective that observers can walk close to a frogmouth in daylight without recognizing it. Nonetheless, frogmouths have been found to be preyed upon by hawks and owls. When adopting the “camouflage posture,” a frogmouth becomes immobile and nearly closes its eyes, thereby masking its salient, bright yellow irides, although it is possible at times to see eye movements behind the partially closed lids. Frogmouths have a single fovea in the temporal retina of each eye. Since this fovea views the frontal visual field, it can be used in cooperation with that of the other eye for binocular vision and consequently is frequently referred to as the “binocular” fovea (Bravo and Pettigrew, 1981; Pettigrew, 1979). The little eagle (Haliaetus morphnoides) is a small, but otherwise typical, eagle of the Accipitridae family of diurnal predators. The following details of the natural history of Haliaetus are from Cramp and Simmons (1981). Like other eagles, the little eagle hunts during the day by soaring aloft where it has a commanding view of the open or semiopen countryside over which it hunts. Prey are taken on the ground after a long dive or, more rarely, in the air. Apart from humans, an adult little eagle has no significant predator. Like other diurnal raptors, eagles have two foveas in each retina, a “binocular fovea” in the temporal retina, and a “monocular fovea” near the optic axis (Wood, 1917). The evolution of the visual system in all species involves a tradeoff between the advantages of a maximally large visual field for panoramic vision and those of a large area of overlap of the two