Adaptive bill morphology for enhanced tool manipulation in New Caledonian crows

Early increased sophistication of human tools is thought to be underpinned by adaptive morphology for efficient tool manipulation. Such adaptive specialisation is unknown in nonhuman primates but may have evolved in the New Caledonian crow, which has sophisticated tool manufacture. The straightness of its bill, for example, may be adaptive for enhanced visually-directed use of tools. Here, we examine in detail the shape and internal structure of the New Caledonian crow’s bill using Principal Components Analysis and Computed Tomography within a comparative framework. We found that the bill has a combination of interrelated shape and structural features unique within Corvus, and possibly birds generally. The upper mandible is relatively deep and short with a straight cutting edge, and the lower mandible is strengthened and upturned. These novel combined attributes would be functional for (i) counteracting the unique loading patterns acting on the bill when manipulating tools, (ii) a strong precision grip to hold tools securely, and (iii) enhanced visually-guided tool use. Our findings indicate that the New Caledonian crow’s innovative bill has been adapted for tool manipulation to at least some degree. Early increased sophistication of tools may require the co-evolution of morphology that provides improved manipulatory skills.

[1]  C. Rutz,et al.  Strong between‐site variation in New Caledonian crows’ use of hook‐tool‐making materials , 2016, Biological journal of the Linnean Society. Linnean Society of London.

[2]  Dieter H. Pahr,et al.  Human-like hand use in Australopithecus africanus , 2015, Science.

[3]  A. Gamauf,et al.  Phylogeographic patterns in widespread corvid birds. , 2007, Molecular phylogenetics and evolution.

[4]  David A. Luther,et al.  The Island Syndrome in Coastal Wetland Ecosystems: Convergent Evolution of Large Bills in Mangrove Passerines , 2011 .

[5]  C. Ward,et al.  Early Pleistocene third metacarpal from Kenya and the evolution of modern human-like hand morphology , 2013, Proceedings of the National Academy of Sciences.

[6]  Christian Rutz,et al.  New Caledonian crows attend to multiple functional properties of complex tools , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  A. Kacelnik,et al.  Behavioural ecology: Tool manufacture by naive juvenile crows , 2005, Nature.

[8]  Jolyon Troscianko,et al.  Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows , 2012, Nature Communications.

[9]  Russell D. Gray,et al.  Species-wide manufacture of stick-type tools by New Caledonian Crows , 2002 .

[10]  C. E. Corbin,et al.  Linkage and trade‐off in trophic morphology and behavioural performance of birds , 2015 .

[11]  Gavin R. Hunt,et al.  Tool Use by the New Caledonian Crow Corvus moneduloides to Obtain Cerambycidae from Dead Wood , 2000 .

[12]  Yusuke Morita,et al.  Technical note: Quantification of neurocranial shape variation using the shortest paths connecting pairs of anatomical landmarks. , 2013, American journal of physical anthropology.

[13]  F. Bookstein,et al.  Semilandmarks in Three Dimensions , 2005 .

[14]  P. O’Higgins.  The study of morphological variation in the hominid fossil record: biology, landmarks and geometry , 2000, Journal of anatomy.

[15]  Christian Rutz,et al.  The evolutionary origins and ecological context of tool use in New Caledonian crows , 2012, Behavioural Processes.

[16]  Walter J. Bock,et al.  Functional and evolutionary morphology of woodpeckers , 1999 .

[17]  Brian G Richmond,et al.  Hand pressure distribution during Oldowan stone tool production. , 2012, Journal of human evolution.

[18]  Walter J. Bock,et al.  An Approach to the Functional Analysis of Bill Shape , 1966 .

[19]  Fred L. Bookstein,et al.  Landmark methods for forms without landmarks: morphometrics of group differences in outline shape , 1997, Medical Image Anal..

[20]  A. Farke,et al.  Femoral Strength and Posture in Terrestrial Birds and Non‐Avian Theropods , 2009, Anatomical record.

[21]  J. D. Hoyo,et al.  Handbook of the Birds of the World , 2010 .

[22]  Yubo Fan,et al.  Why Do Woodpeckers Resist Head Impact Injury: A Biomechanical Investigation , 2011, PloS one.

[23]  P. O'higgins,et al.  Facial growth in Cercocebus torquatus: an application of three‐dimensional geometric morphometric techniques to the study of morphological variation , 1998, Journal of anatomy.

[24]  Peter R Grant,et al.  Two developmental modules establish 3D beak-shape variation in Darwin's finches , 2011, Proceedings of the National Academy of Sciences.

[25]  C. Ruff,et al.  Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation. , 2006, American journal of physical anthropology.

[26]  P. Aerts,et al.  Mechanical stress, fracture risk and beak evolution in Darwin's ground finches (Geospiza) , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  Russell D. Gray,et al.  Direct observations of pandanus-tool manufacture and use by a New Caledonian crow (Corvus moneduloides) , 2004, Animal Cognition.

[28]  P. Grant.  Bill size, body size, and the ecological adaptations of bird species to competitive situations on islands. , 1968, Systematic zoology.

[29]  Sabine Tebbich,et al.  The ecology of tool-use in the woodpecker finch (Cactospiza pallida) , 2002 .

[30]  E. Menzel.  Animal Tool Behavior: The Use and Manufacture of Tools by Animals, Benjamin B. Beck. Garland STPM Press, New York and London (1980), 306, Price £24.50 , 1981 .

[31]  M W Marzke,et al.  Precision grips, hand morphology, and tools. , 1997, American journal of physical anthropology.

[32]  Neil T. Roach,et al.  Elastic energy storage in the shoulder and the evolution of high-speed throwing in Homo , 2013, Nature.

[33]  Martin Irestedt,et al.  Brains, tools, innovation and biogeography in crows and ravens , 2012, BMC Evolutionary Biology.

[34]  G. Hunt.  Manufacture and use of hook-tools by New Caledonian crows , 1996, Nature.

[35]  Hiroshi Matsui,et al.  Involvement of vision in tool use in crow , 2014, Neuroreport.

[36]  Russell D Gray,et al.  The crafting of hook tools by wild New Caledonian crows , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  P. Wilson,et al.  Energetics of South Island kaka (Nestor meridionalis meridionalis) feeding on the larvae of kanuka longhorn beetles (Ochrocydus huttoni) , 1987 .

[38]  G. Hunt,et al.  Cognitive requirements for tool use by New Caledonian crows (Corvus moneduloides) , 2007 .

[39]  R. Danner,et al.  A critical season approach to Allen's rule: bill size declines with winter temperature in a cold temperate environment , 2015 .

[40]  Naomichi Ogihara,et al.  Three-dimensional endocranial shape variation in the modern Japanese population , 2015 .

[41]  Christian Rutz,et al.  Tool use by wild New Caledonian crows Corvus moneduloides at natural foraging sites , 2010, Proceedings of the Royal Society B: Biological Sciences.

[42]  Alex H. Taylor,et al.  Cognitive insights from tool use in nonhuman animals. , 2017 .

[43]  C. Cunningham.  Tool Use in Animals. Cognition and Ecology Crickette M. Sanz Josep , 2013, Animal Behaviour.

[44]  Mamoru Hosaka,et al.  Modeling of Curves and Surfaces in CAD/CAM , 1992, Computer Graphics — Systems and Applications.

[45]  Gavin R Hunt,et al.  Lateralized tool use in wild New Caledonian crows , 2004, Animal Behaviour.

[46]  G. Hunt,et al.  Why is tool use rare in animals , 2013 .

[47]  G. Hunt,et al.  Diversification and cumulative evolution in New Caledonian crow tool manufacture , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  B. Beck.  Animal Tool Behavior: The Use and Manufacture of Tools by Animals , 1980 .