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

2014; Elsevier BV; Volume: 24; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2014.10.035

1879-0445

Antone Martinho, Zackory T. Burns, Auguste M. P. von Bayern, Alex Kacelnik,

Animal Behavior and Reproduction

Tool use, though rare, is taxonomically widespread, but morphological adaptations for tool use are virtually unknown [1Shumaker R.W. Walkup K.R. Beck B.B. Animal Tool Behavior: The Use and Manufacture of Tools by Animals. JHU Press, Baltimore2011Google Scholar]. We focus on the New Caledonian crow (NCC, Corvus moneduloides), which displays some of the most innovative tool-related behavior among nonhumans [2Hunt G.R. Manufacture and use of hook-tools by New Caledonian crows.Nature. 1996; 379: 249-251Google Scholar, 3Hunt G.R. Gray R.D. Diversification and cumulative evolution in New Caledonian crow tool manufacture.Proc. Biol. Sci. 2003; 270: 867-874Google Scholar, 4McGrew W.C. Is primate tool use special? Chimpanzee and New Caledonian crow compared.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013; 368: 20120422Google Scholar, 5Troscianko J. von Bayern A.M.P. Chappell J. Rutz C. Martin G.R. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.Nat Commun. 2012; 3: 1110Google Scholar, 6Rutz C. St Clair J.J.H. The evolutionary origins and ecological context of tool use in New Caledonian crows.Behav. Processes. 2012; 89: 153-165Google Scholar]. One of their major food sources is larvae extracted from burrows with sticks held diagonally [7Rutz C. Bluff L.A. Reed N. Troscianko J. Newton J. Inger R. Kacelnik A. Bearhop S. The ecological significance of tool use in New Caledonian crows.Science. 2010; 329: 1523-1526Google Scholar] in the bill, oriented with individual, but not species-wide, laterality [8Weir A.A.S. Kenward B. Chappell J. Kacelnik A. Lateralization of tool use in New Caledonian crows (Corvus moneduloides).Proc. Biol. Sci. 2004; 271: S344-S346Google Scholar, 9Rutledge R. Hunt G.R. Lateralized tool use in wild New Caledonian crows.Anim. Behav. 2004; 67: 327-332Google Scholar]. Among possible behavioral [10Kenward B. Weir A.A.S. Rutz C. Kacelnik A. Behavioural ecology: tool manufacture by naive juvenile crows.Nature. 2005; 433 (121–121)Google Scholar] and anatomical adaptations for tool use [5Troscianko J. von Bayern A.M.P. Chappell J. Rutz C. Martin G.R. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.Nat Commun. 2012; 3: 1110Google Scholar, 11Delacour J. Guide des oiseaux de la Nouvelle-Calédonie et de ses dépendances. Delachaux et Niestlé SA, Neuchâtel1966Google Scholar, 12Jollie M. Phylogeny of the species of Corvus.Biologist. 1978; 60: 73-108Google Scholar, 13Goodwin D. Crows of the World. British Museum, London1986Google Scholar, 14Doughty C. Day N. Plant A. Birds of the Solomons, Vanuatu & New Caledonia. A & C Black, London1999Google Scholar, 15Kenward B. Rutz C. Weir A.A.S. Chappell J. Kacelnik A. Morphology and sexual dimorphism of the New Caledonian crow Corvus moneduloides, with notes on its behaviour and ecology.Ibis. 2004; 146: 652-660Google Scholar], NCCs possess unusually wide binocular visual fields (up to 60°), suggesting that extreme binocular vision may facilitate tool use [5Troscianko J. von Bayern A.M.P. Chappell J. Rutz C. Martin G.R. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.Nat Commun. 2012; 3: 1110Google Scholar]. 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 [5Troscianko J. von Bayern A.M.P. Chappell J. Rutz C. Martin G.R. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.Nat Commun. 2012; 3: 1110Google Scholar, 16Martin G.R. What is binocular vision for? A birds' eye view.J. Vis. 2009; 9: 1-19Google Scholar]. 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 [17Bourassa D. Handedness and eye-dominance: a meta-analysis of their relationship. Laterality: asymmetries of body.Brain Cogn. 1996; 1: 5-34Google Scholar], 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.