Monocular Tool Control, Eye Dominance, and Laterality in New Caledonian Crows

Abstract

Tool use, though rare, is taxonomically widespread, but morphological adaptations for tool use are virtually unknown. We focus on the New Caledonian crow (NCC, Corvus moneduloides), which displays some of the most innovative tool-related behavior among nonhumans. One of their major food sources is larvae extracted from burrows with sticks held diagonally in the bill, oriented with individual, but not species-wide, laterality. Among possible behavioral and anatomical adaptations for tool use, NCCs possess unusually wide binocular visual fields (up to 60°), suggesting that extreme binocular vision may facilitate tool use. Here, we establish that during natural extractions, tool tips can only be viewed by the contralateral eye. Thus, maintaining binocular view of tool tips is unlikely to have selected for wide binocular fields; the selective factor is more likely to have been to allow each eye to see far enough across the midsagittal line to view the tool's tip monocularly. Consequently, we tested the hypothesis that tool side preference follows eye preference and found that eye dominance does predict tool laterality across individuals. This contrasts with humans' species-wide motor laterality and uncorrelated motor-visual laterality, possibly because bill-held tools are viewed monocularly and move in concert with eyes, whereas hand-held tools are visible to both eyes and allow independent combinations of eye preference and handedness. This difference may affect other models of coordination between vision and mechanical control, not necessarily involving tools.

Lateralized Eye Use Towards Video Stimuli in Bearded Dragons (Pogona vitticeps)

“…Lateralized eye use has been observed in a wide variety of vertebrate species, including mammals (Braccini, Lambeth, Schapiro, & Fitch, 2012;Guo, Meints, Hall, Hall, & Mills, 2009;Racca, Guo, Meints, & Mills, 2012;Smith, Proops, Grounds, Wathan, & McComb, 2016;Versace, Morgante, Pulina, & Vallortigara, 2007), birds (Martinho, Burns, Von Bayern, & Kacelnik, 2014;McKenzie, Andrew, & Jones, 1998;Rogers, 2012;Ventolini et al, 2005;Zucca & Sovrano, 2008), reptiles (Bonati & Csermely, 2011;Hews & Worthington, 2001;Robins, Chen, Beazley, & Dunlop, 2005), amphibians (Vallortigara, Rogers, Bisazza, Lippolis, & Robins, 1998), and fish (Bisazza, De Santi, & Vallortigara, 1999;Bisazza, Facchin, Pignatti, & Vallortigara, 1998;Karenina, Giljov, & Malashichev, 2013). In vertebrates, the right brain hemisphere (which processes information obtained by the left eye) is thought to control emotions and spatial perception, while the left hemisphere (right eye) is responsible for attention, perceptual processing and the control of motor responses (Rogers, Vallortigara, & Andrew, 2013;Vallortigara, Chiandetti, & Sovrano, 2011).…”

Avian binocular vision: It’s not just about what birds can see, it’s also about what they can’t

“…Bird species that use tools, such as New Caledonian crows ( Corvus moneduloides ) and American crows ( Corvus brachyrhynchos ), have particularly wide binocular fields and can see their beak tips [20,21]; hence, their anterior blind areas are small. In the case of the New Caledonian crow, seeing along the shaft of the tool appears to be the key (rather than binocular vision) for using tools to extract food from long, narrow holes in wood [21,43]. When the tool is being used inside a narrow hole, it is held at an angle so that there is an ipsilateral eye and a contralateral eye, but only the contralateral eye can see the tool tip [43].…”

“…In the case of the New Caledonian crow, seeing along the shaft of the tool appears to be the key (rather than binocular vision) for using tools to extract food from long, narrow holes in wood [21,43]. When the tool is being used inside a narrow hole, it is held at an angle so that there is an ipsilateral eye and a contralateral eye, but only the contralateral eye can see the tool tip [43]. Without a wide binocular field that can see the beak tip, the crow would not be able to see the tool tip at all.…”

A complex adaptive system may be essential for cumulative modifications in tool design

“…NC crows also have the widest binocular field of view known in birds, which was suggested to facilitate efficient tool manipulation when searching for prey (Troscianko et al, 2012). Martinho et al (2014) subsequently reported that the wide binocular field enhanced monocular viewing of the tool tip when probing in holes. The wide binocular field allows, for example, the right eye to view the tool tip when it is positioned across the mid-sagittal line on the opposite side of the head.…”