Abstract
Only a handful of bird species are known to use foraging tools in the wild1. Amongst them, the New Caledonian crow (Corvus moneduloides) stands out with its sophisticated tool-making skills2,3. Despite considerable speculation, the evolutionary origins of this species’ remarkable tool behaviour remain largely unknown, not least because no naturally tool-using congeners have yet been identified that would enable informative comparisons4. Here we show that another tropical corvid, the ‘Alalā (C. hawaiiensis; Hawaiian crow), is a highly dexterous tool user. Although the ‘Alalā became extinct in the wild in the early 2000s, and currently survives only in captivity5, at least two lines of evidence suggest that tool use is part of the species’ natural behavioural repertoire: juveniles develop functional tool use without training, or social input from adults; and proficient tool use is a species-wide capacity. ‘Alalā and New Caledonian crows evolved in similar environments on remote tropical islands, yet are only distantly related6, suggesting that their technical abilities arose convergently. This supports the idea that avian foraging tool use is facilitated by ecological conditions typical of islands, such as reduced competition for embedded prey and low predation risk4,7. Our discovery creates exciting opportunities for comparative research on multiple tool-using and non-tool-using corvid species. Such work will in turn pave the way for replicated cross-taxonomic comparisons with the primate lineage, enabling valuable insights into the evolutionary origins of tool-using behaviour.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Self-care tooling innovation in a disabled kea (Nestor notabilis)
Scientific Reports Open Access 10 September 2021
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
References
Shumaker, R. W., Walkup, K. R. & Beck, B. B. Animal Tool Behavior: the Use and Manufacture of Tools by Animals (Johns Hopkins Univ. Press, 2011)
Hunt, G. R. Manufacture and use of hook-tools by New Caledonian crows. Nature 379, 249–251 (1996)
Klump, B. C., Sugasawa, S., St Clair, J. J. H. & Rutz, C. Hook tool manufacture in New Caledonian crows: behavioural variation and the influence of raw materials. BMC Biol. 13, 97 (2015)
Rutz, C. & St Clair, J. J. H. The evolutionary origins and ecological context of tool use in New Caledonian crows. Behav. Processes 89, 153–165 (2012)
Banko, P. C., Ball, D. L. & Banko, W. E. in The Birds of North America, vol. 17 (eds Poole, A. & Gill, F. ) (The Birds of North America, Inc., 2002)
Haring, E., Däubl, B., Pinsker, W., Kryukov, A. & Gamauf, A. Genetic divergences and intraspecific variation in corvids of the genus Corvus (Aves: Passeriformes: Corvidae) – a first survey based on museum specimens. J. Zool. Syst. Evol. Res. 50, 230–246 (2012)
Tebbich, S. & Teschke, I. in Tool Use in Animals: Cognition and Ecology. (eds Sanz, C. M., Call, J. & Boesch, C. ) (Cambridge Univ. Press, 2013)
del Hoyo, J., Elliott, A. & Christie, D. A. (eds) Handbook of the Birds of the World. Bush-shrikes to Old World Sparrows, vol. 14 (Lynx Edicions, 2009)
Troscianko, 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. 3, 1110 (2012)
Goodwin, D. Crows of the World (British Museum, 1976)
U.S. Fish and Wildlife Service (USFWS). Revised Recovery Plan for the ‘Alalaˉ (Corvus hawaiiensis) (USFWS, 2009)
Faike, E. Wild voices in captivity: the fate of the ‘Alala. Birding 38, 64–67 (2006)
Smith, M. ‘Alala: weighing in. http://blog.sandiegozooglobal.org/2011/10/21/alala-weighing-in/ (2011)
Matsui, H. et al. Adaptive bill morphology for enhanced tool manipulation in New Caledonian crows. Sci. Rep. 6, 22776 (2016)
Kenward, B., Weir, A. A. S., Rutz, C. & Kacelnik, A. Tool manufacture by naive juvenile crows. Nature 433, 121 (2005)
Kenward, B., Rutz, C., Weir, A. A. S. & Kacelnik, A. Development of tool use in New Caledonian crows: inherited action patterns and social influences. Anim. Behav. 72, 1329–1343 (2006)
Kenward, B. et al. On the evolutionary and ontogenetic origins of tool-oriented behaviour in New Caledonian crows (Corvus moneduloides). Biol. J. Linn. Soc. 102, 870–877 (2011)
Mesoudi, A., Chang, L., Dall, S. R. X. & Thornton, A. The evolution of individual and cultural variation in social learning. Trends Ecol. Evol. 31, 215–225 (2016)
Tennie, C., Call, J. & Tomasello, M. Ratcheting up the ratchet: on the evolution of cumulative culture. Phil. Trans. R. Soc. B 364, 2405–2415 (2009)
Bird, C. D. & Emery, N. J. Insightful problem solving and creative tool modification by captive nontool-using rooks. Proc. Natl Acad. Sci. USA 106, 10370–10375 (2009)
Sakai, H. F., Ralph, C. J. & Jenkins, C. D. Foraging ecology of the Hawaiian crow, an endangered generalist. Condor 88, 211–219 (1986)
Walters, M. J. Seeking the Sacred Raven (Island Press, 2006)
Troscianko, J. & Rutz, C. Activity profiles and hook-tool use of New Caledonian crows recorded by bird-borne video cameras. Biol. Lett. 11, 20150777 (2015)
Pratt, T. K., Atkinson, C. T., Banko, P. C., Jacobi, J. D. & Woodworth, B. L. (eds) Conservation Biology of Hawaiian Forest Birds (Yale Univ. Press, 2009)
Tebbich, S., Seed, A. M., Emery, N. J. & Clayton, N. S. Non-tool-using rooks, Corvus frugilegus, solve the trap-tube problem. Anim. Cogn. 10, 225–231 (2007)
James, H. F. & Olson, S. L. Descriptions of thirty-two new species of birds from the Hawaiian Islands: Part II. Passeriformes. Ornithol. Monogr. 46, 1–88 (1991)
Darwin, C. R. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871)
Goodall, J. Tool-using and aimed throwing in a community of free-living chimpanzees. Nature 201, 1264–1266 (1964)
Hoeck, P. E. A., Wolak, M. E., Switzer, R. A., Kuehler, C. M. & Lieberman, A. A. Effects of inbreeding and parental incubation on captive breeding success in Hawaiian crows. Biol. Conserv. 184, 357–364 (2015)
Banko, P. C. in Conservation Biology of Hawaiian Forest Birds (eds Pratt, T. K., Atkinson, C. T., Banko, P. C., Jacobi, J. D. & Woodworth, B. L. ) (Yale Univ. Press, 2009)
National Research Council (NRC). The Scientific Bases for the Preservation of the Hawaiian Crow (National Academy Press, 1992)
Hedrick, P. W., Hoeck, P. E. A., Fleischer, R. C., Farabaugh, S. & Masuda, B. M. The influence of captive breeding management on founder representation and inbreeding in the ‘Alalaˉ, the Hawaiian crow. Conserv. Genet. 17, 369–378 (2016)
Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998)
Harvey, N. N., Farabaugh, S. M. & Druker, B. B. Effects of early rearing experience on adult behavior and nesting in captive Hawaiian crows (Corvus hawaiiensis). Zoo Biol. 21, 59–75 (2002)
Péter, A. Solomon Coder (version beta14.03.10): A Simple Solution for Behavior Coding. http://solomoncoder.com (2011)
Mameli, M. & Bateson, P. An evaluation of the concept of innateness. Phil. Trans. R. Soc. B 366, 436–443 (2011)
Kuehler, C., Kuhn, M., McIlraith, B. & Campbell, G. Artificial incubation and hand-rearing of ‘Alala (Corvus hawaiiensis) eggs removed from the wild. Zoo Biol. 13, 257–266 (1994)
Culliney, S., Pejchar, L., Switzer, R. & Ruiz-Gutierrez, V. Seed dispersal by a captive corvid: the role of the ‘Alalaˉ (Corvus hawaiiensis) in shaping Hawai‘i’s plant communities. Ecol. Appl. 22, 1718–1732 (2012)
Blumstein, D. T. & Daniel, J. C. Quantifying Behavior the JWatcher Way (Sinauer Associates, 2007)
R Development Core Team. R: A Language and Environment for Statistical Computing. http://www.R-project.org (2014)
St Clair, J. J. H. et al. Experimental resource pulses influence social-network dynamics and the potential for information flow in tool-using crows. Nat. Commun. 6, 7197 (2015)
Auersperg, A. M. et al. Social transmission of tool use and tool manufacture in Goffin cockatoos (Cacatua goffini). Proc. R. Soc. B 281, 20140972 (2014)
Hobaiter, C., Poisot, T., Zuberbühler, K., Hoppitt, W. & Gruber, T. Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees. PLoS Biol. 12, e1001960 (2014)
Gori, F., Folino, G., Jetten, M. S. M. & Marchiori, E. MTR: taxonomic annotation of short metagenomic reads using clustering at multiple taxonomic ranks. Bioinformatics 27, 196–203 (2011)
Hoppitt, W. & Laland, K. N. Social Learning: An Introduction to Mechanisms, Methods and Models (Princeton Univ. Press, 2013)
Jønsson, K. A., Fabre, P.-H. & Irestedt, M. Brains, tools, innovation and biogeography in crows and ravens. BMC Evol. Biol. 12, 72 (2012)
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013)
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)
Fleischer, R. C. & McIntosh, C. E. Molecular systematics and biogeography of the Hawaiian avifauna. Stud. Avian Biol. 22, 51–60 (2001)
Gibbs, H. L. & Grant, P. R. Oscillating selection on Darwin’s finches. Nature 327, 511–513 (1987)
Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015)
Tebbich, S., Taborsky, M., Fessl, B. & Dvorak, M. The ecology of tool-use in the woodpecker finch (Cactospiza pallida). Ecol. Lett. 5, 656–664 (2002)
Morse, D. H. The use of tools by brown-headed nuthatches. Wilson Bull. 80, 220–224 (1968)
Visalberghi, E. & Fragaszy, D. in Tool Use in Animals: Cognition and Ecology (eds Sanz, C. M., Call, J. & Boesch, C. ) (Cambridge Univ. Press, 2013)
Acknowledgements
We thank: the many people – far too many to name individually – who have prevented the ‘Alalaˉ’s extinction, and who are working tirelessly towards its successful reintroduction into the wild; R. Fleischer for facilitating initial contacts; San Diego Zoo Global’s staff for assistance with experiments; C. Higgott for help with video scoring; D. Parker for constructing the consensus phylogeny; several photographers for providing images for Fig. 1; S. Thompson for help with graphic design; and G. Ruxton for statistical advice. Research was conducted with permission from San Diego Zoo Global’s IACUC animal welfare committee (Project ID#12-017), and with funding from the Biotechnology and Biological Sciences Research Council, UK (BBSRC; grant BB/G023913/2 to C.R., and studentship to B.C.K.), the University of St Andrews (C.R.), JASSO (S.S.), and the Royal Society of London (M.B.M.). Funding for the captive ‘Alala¯ propagation programme was provided by the U.S. Fish and Wildlife Service, Hawai‘i Division of Forestry and Wildlife, Moore Family Foundation, Marisla Foundation, several anonymous donors, and San Diego Zoo Global.
Author information
Authors and Affiliations
Contributions
C.R. conceived of, initiated and led the project, and secured funding; R.A.S. and B.M.M. led the captive ‘Alalaˉ propagation programme, with support from R.L., J.K. and L.K.; C.R., J.J.H.S.C. and B.C.K. designed behavioural experiments; B.C.K., J.J.H.S.C. and C.R. conducted the species-wide tool-use assay, and L.K. performed the ontogeny experiment, with help from R.L., C.R., J.J.H.S.C. and B.C.K.; B.C.K. scored videos and extracted behavioural data, except for ontogeny trials, which were scored by S.W. and processed by S.S.; L.K., J.K., B.M.M. and C.R. collated and checked data on the life histories of captive birds; M.B.M. and B.C.K. assessed bird-performance data; R.J. and C.R. conducted social-diffusion simulations; C.R. and B.C.K. coordinated manuscript preparation, analysed data and prepared figures and videos; and C.R. wrote the manuscript, which was edited by B.C.K., J.J.H.S.C., R.J. and B.M.M., and approved by all co-authors.
Corresponding author
Ethics declarations
Competing interests
The authors declare the following competing financial interests: five co-authors were (R.L., J.K., R.A.S.), or still are (L.K., B.M.M.), employees of San Diego Zoo Global, which is a not-for-profit organisation.
Additional information
Reviewer Information Nature thanks T. Bugnyar, B. Kenward, S. Tebbich and the other anonymous reviewer(s) for their contribution to the peer review of this work.
Extended data figures and tables
Extended Data Figure 1 Craniofacial morphology of tool-using ‘Alalā and New Caledonian crows.
a, Although some other Corvus species8 have relatively straight bills—in terms of culmen- and commissural-line projections—they usually lack the pronounced distal angle of the gonys that is characteristic of the tool-using (i) ‘Alalā (adult female #191, 8 January 2015) and (ii) New Caledonian crow (adult female #CR6, 6 October 2013; photo: P. Barros da Costa), and also have larger distal protrusions of the upper mandible. Despite the overall similarity of the two species4,10, ‘Alalā are larger and more robust birds (Fig. 1c, d), and exhibit modest bill curvature, relatively smaller eyes, and notable intraspecific variation in bill shape. The scale bar applies to all four images. b, ‘Alalā have markedly forward-pointing eyes, with high lateral eye-movement amplitudes, enabling (i) a considerable degree of convergence (#96, 17 February 2014; note that the red-brown plumage colouration is an image artefact; no adjustments have been made). The movement of (ii) both eyes (#201, 9 August 2014), or (iii) just one eye (red arrow; #206, 9 August 2014), can often be observed during the handling of birds for routine health checks (the white marker on the bills is a removable scale bar; see Supplementary Video 5). Although the ‘Alalā’s visual field could not be measured in this study (see Methods), these features are likely to produce a large field of binocular overlap, which in New Caledonian crows is thought to aid tool manufacture and deployment9. c, When ‘Alalā hold stick tools in a transverse grip, (i) the slight curvature of the birds’ bill can force the non-functional end of the tool close to the eye (as would be predicted from earlier work; see figure 5 in ref. 9, ii) which may cause discomfort or even injury (red arrow indicates nictitating membrane, which the bird closed temporarily to protect its eye); (iii) this may explain why the vast majority of individuals prefer to hold tools in a frontal grip (adult male #134, 21 January 2013; transverse grip observed in only 11 of 104 subjects tested on the standardized log task).
Extended Data Figure 2 Food-extraction tasks for investigating tool-use behaviour in captive ‘Alalā.
a, A species-wide assay of tool-use competence was conducted by presenting birds with a baited Koa Acacia koa log (length, ~78 cm; diameter, ~16 cm), containing two vertical holes (depth, ~5.0 cm; diameter, ~2.3 cm), two horizontal holes (~5.4 cm; ~2.3 cm), one vertical crevice (width × depth, ~2.4 × 6.4 cm) and one horizontal crevice (height × depth, ~2.3 × 6.8 cm); all estimates of dimensions are averages for the two log set-ups used in experimental trials (see Methods). Sticks for potential tool use were scattered in front of the log (length classes: 3 of 0–5 cm; 3 of 10–15 cm; 3 of 20–25 cm; and 3 of 30–35 cm), and assorted plant materials for potential tool manufacture were provided on a wooden stand nearby (KBCC: 2 ‘Ōhi‘a lehua Metrosideros polymorpha stems, 2 Koa stems, 1 fern frond, 2 dead branched stems; MBCC: 2 dead branched stems). As subjects had access to suitable tools during trials, current data probably underestimate the species’ tool-making capabilities. b, The tool-use competence of seven juvenile birds was assessed once per week (and more often towards the end of the study period; see Methods), using a baited wooden platform (~50 × 50 cm) with four vertical holes (depth, ~4.5–5.4 cm; diameter, ~2.0–2.7 cm) and two vertical crevices (width × length × height, ~2.5 × 21.2 × 7.3 cm and ~2.4 × 13.5 × 8.0 cm). From late January 2013 onwards, a second replica platform was used to enable parallel testing of both experimental groups. During the final stages of the experiment, the four vertical holes were substituted with horizontal holes (by rotating the wooden blocks), and two horizontal crevices were added (not shown here; see Supplementary Video 3).
Supplementary information
Spontaneous tool behaviour by an ‘Alalā
This unedited scene shows the first presentation of the log set-up to adult male #134 (21 January 2013). Note that the log is a prototype that, compared to the final design later used for the species-wide behavioural assay, contained two additional holes. (MP4 28134 kb)
Tool selectivity, modification and manufacture in ‘Alalā
During experimental trials, many ‘Alalā were observed: a, to choose tools of appropriate dimensions; b, to replace tools that were not suitable; c, to transport non-supplied sticks to the set-up to be used as tools; to modify tools d, before or e, during deployment; or f, to handle, try and modify several different sticks during an extraction attempt. Tool manufacture behaviour included: g, snipping-off twigs from supplied dead branches; the production of h, bark flakes and i, wood splinters; and j, successive subtraction of material from non-supplied live plant material. (MP4 27705 kb)
Ontogeny of tool-related behaviour in naïve juvenile ‘Alalā
Functional tool behaviour can result from (a combination of) genetic predispositions, social learning, and individual learning. To investigate the relative importance of different processes, ‘naïve’ juveniles can be reared in captivity without opportunities to observe tool-use behaviour in proficient adult conspecifics, or even in humans. Under such controlled conditions, ‘Alalā chicks develop functional tool use over the first few months of life: a, first handling and carrying objects, including sticks, stones and other items; before b, inserting them into holes and crevices with gradually increasing proficiency (here, during a probe trial with several baited extraction tasks presented on a ‘platform’). (MP4 29544 kb)
Historical recordings of ‘Alalā using tools
Before the commencement of systematic behavioural experiments, staff at the KBCC and MBCC facilities had regularly observed ‘Alalā using tools. Following these opportunistic observations, on the 28 July 2011, four different birds were filmed using tools to reach for bait placed in a water bath (#114, #118, #135), or behind wire mesh (#146). (MP4 27114 kb)
Eye movements in an ‘Alalā
Like New Caledonian crows, ‘Alalā have unusually large eye-movement amplitudes. This video was taken when adult male #121 was trapped for a routine pre-breeding health check (19 March 2015) and presented with a neonate mouse to attract its attention. (MP4 28952 kb)
Tool-use behaviour in crows
Tool use of an adult male a, ‘Alalā and b, New Caledonian crow. ‘Alalā tend to hold stick tools in a frontal grip whereas New Caledonian crows prefer a transverse grip. c, Naturally non-tool-using rooks can be trained to use tools, but compared to most ‘Alalā and New Caledonian crows, they appear to handle sticks less dexterously (but note difference in extraction tasks provided). (MP4 25657 kb)
Rights and permissions
About this article
Cite this article
Rutz, C., Klump, B., Komarczyk, L. et al. Discovery of species-wide tool use in the Hawaiian crow. Nature 537, 403–407 (2016). https://doi.org/10.1038/nature19103
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature19103
This article is cited by
-
Higher Cognitive Abilities in Birds: A Comparative Evolutionary Analysis
Neuroscience and Behavioral Physiology (2022)
-
Self-care tooling innovation in a disabled kea (Nestor notabilis)
Scientific Reports (2021)
-
Hook innovation boosts foraging efficiency in tool-using crows
Nature Ecology & Evolution (2018)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.
