Discovery of species-wide tool use in the Hawaiian crow

Journal name:
Nature
Volume:
537,
Pages:
403–407
Date published:
DOI:
doi:10.1038/nature19103
Received
Accepted
Published online

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.

At a glance

Figures

  1. Phylogenetic and biogeographical context of tool behaviour in crows.
    Figure 1: Phylogenetic and biogeographical context of tool behaviour in crows.

    a, Phylogeny for the genus Corvus (blue circles, posterior probabilities ≥ 0.90). Scale bar: estimated substitutions per site. b, Variation in craniofacial morphology (adapted from ref. 8, Lynx Edicions). c, One of the last wild ‘Alalā (27 February 1998, Kealakekua, Hawai‘i; photo: Jack Jeffrey Photography). d, New Caledonian crow (photo: M. Griffioen). e, Location of Hawai‘i and New Caledonia (globe: Google Earth, NASA, US Geological Survey). f, Hawaiian corvids (skulls adapted from ref. 26, American Ornithologists’ Union; photo: C.R.), and historical ‘Alalā distribution (from ref. 11, USFWS). † denotes extinct species. g, Discovery timeline for well-known habitual avian tool users (photos: A. Gandolfi/naturepl.com; D. Pintimalli; D. Brinkhuizen; J. Troscianko), with landmark chimpanzee reports by Darwin27 and Goodall28 for reference.

  2. Species-wide tool-use behaviour in ‘Alalā.
    Figure 2: Species-wide tool-use behaviour in ‘Alalā.

    a, Captive birds using stick tools to extract bait from experimental logs. b, Development of the world’s ‘Alalā population and results of species-wide tool-use assay (birds shown survived at least until post-fledging age; inset data from ref. 29, Elsevier). ce, Tool-use competence across: c, sexes (M, male; F, female) and facilities (KBCC, Keauhou Bird Conservation Center; MBCC, Maui Bird Conservation Center; subdivided according to where subjects were raised and tested); d, age classes; and e, different test conditions (tested individually or in a group). f, g, Bird performance: f, outcome of trials and g, extraction speed for different tasks. Panels bg refer to the standardized tool-use assay (Extended Data Fig. 2a); g only includes successful extractions from the first individual trial where birds used tools.

  3. Development of tool-use behaviour in naive, juvenile ‘Alalā.
    Figure 3: Development of tool-use behaviour in naive, juvenile ‘Alalā.

    a, Object-handling rates (bill only) estimated from focal-bird observations (week 1 commenced 3 September 2012; ‘sticks’ are all stick-type objects, fern sections and branched pieces of plant; correlation coefficients). b, Group A on experimental platform. c, Behavioural development as documented through weekly probe trials, from week 3 onward (action types are defined in Extended Data Table 1; for ①–③, see Methods). d, Comparison of object-manipulation times (bill, and foot-grasped17) 3–5 weeks post-fledging (weekly means; note that n<5 birds for some values) between ‘Alalā, New Caledonian (NC) crows17 and non-tool-using ravens17. e, Potential for social diffusion across the ‘Alalā contact network (1996–2013, cumulative results; hatching blocks out the 7 isolated subjects of the rearing experiment): co-housing matrix (left) and reachability matrix (right).

  4. Craniofacial morphology of tool-using ‘Alalā and New Caledonian crows.
    Extended Data Fig. 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).

  5. Food-extraction tasks for investigating tool-use behaviour in captive ‘Alalā.
    Extended Data Fig. 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).

Tables

  1. Behavioural actions scored for captive, juvenile ‘Alalaˉ during standardized probe trials
    Extended Data Table 1: Behavioural actions scored for captive, juvenile ‘Alalaˉ during standardized probe trials
  2. Observation rates of tool behaviour for three naturally tool-using bird species
    Extended Data Table 2: Observation rates of tool behaviour for three naturally tool-using bird species

Videos

  1. Spontaneous tool behaviour by an Alal
    Video 1: 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.
  2. Tool selectivity, modification and manufacture in Alal
    Video 2: 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.
  3. Ontogeny of tool-related behaviour in naïve juvenile Alal
    Video 3: 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’).
  4. Historical recordings of Alal using tools
    Video 4: 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).
  5. Eye movements in an Alal
    Video 5: 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.
  6. Tool-use behaviour in crows
    Video 6: 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).

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Author information

Affiliations

  1. Centre for Biological Diversity, School of Biology, University of St Andrews, Sir Harold Mitchell Building, St Andrews KY16 9TH, UK

    • Christian Rutz,
    • Barbara C. Klump,
    • Saskia Wischnewski,
    • Shoko Sugasawa,
    • Michael B. Morrissey &
    • James J. H. St Clair
  2. Institute for Conservation Research, San Diego Zoo Global, PO Box 39, Volcano, Hawai‘i 96785, USA

    • Lisa Komarczyk,
    • Rosanna Leighton &
    • Bryce M. Masuda
  3. Institute for Conservation Research, San Diego Zoo Global, 2375 Olinda Road, Makawao, Hawai‘i 96768, USA

    • Joshua Kramer
  4. Department of Physics and Centre for Networks and Collective Behaviour, University of Bath, Bath BA2 7AY, UK

    • Richard James
  5. Institute for Conservation Research, San Diego Zoo Global, 15600 San Pasqual Valley Road, Escondido, California 92027, USA

    • Richard A. Switzer

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.

Competing financial 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.

Corresponding author

Correspondence to:

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.

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Craniofacial morphology of tool-using ‘Alalā and New Caledonian crows. (864 KB)

    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).

  2. Extended Data Figure 2: Food-extraction tasks for investigating tool-use behaviour in captive ‘Alalā. (902 KB)

    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).

Extended Data Tables

  1. Extended Data Table 1: Behavioural actions scored for captive, juvenile ‘Alalaˉ during standardized probe trials (138 KB)
  2. Extended Data Table 2: Observation rates of tool behaviour for three naturally tool-using bird species (40 KB)

Supplementary information

Video

  1. Video 1: Spontaneous tool behaviour by an ‘Alalā (27.47 MB, Download)
    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.
  2. Video 2: Tool selectivity, modification and manufacture in ‘Alalā (27.05 MB, Download)
    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.
  3. Video 3: Ontogeny of tool-related behaviour in naïve juvenile ‘Alalā (28.85 MB, Download)
    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’).
  4. Video 4: Historical recordings of ‘Alalā using tools (26.47 MB, Download)
    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).
  5. Video 5: Eye movements in an ‘Alalā (28.27 MB, Download)
    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.
  6. Video 6: Tool-use behaviour in crows (25.05 MB, Download)
    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).

Additional data