Visual-field measurements

We used a well-established ophthalmoscopic reflex technique to measure visual-field parameters (monocular, binocular and cyclopean fields) and eye-movement amplitudes in 18 alert subjects across 6 Corvus species (Table 1). This technique has been used in excess of 30 years on 46 bird species of different phylogeny, ecology and behaviour, permitting standardized interspecific comparisons7. The procedure is non-invasive and follows guidelines established by the United Kingdom's Animals (Scientific Procedures) Act (1986) and the Animal Welfare Act (2006).

To locate subjects suitable for experimentation, we conducted an extensive search, using both our personal contacts and information found on the internet. We considered all species of the genus Corvus, and our final sample (Table 1) reflects what could be achieved within the logistical constraints of our study. All experimental subjects were captive animals in the UK, Germany or Austria, with the exception of two ravens that were caught near the Konrad Lorenz Research Station in Grünau, Austria, as part of an ongoing field project. These two individuals were released back into the wild immediately after testing and marking. All other subjects were immediately returned to their home aviaries once measured.

Each bird was held securely in a foam rubber cradle using fabric hook-and-loop fastener straps that wrap upon themselves (Supplementary Fig. S1). The feet and legs were carefully tucked away beneath the bird, and the head was held in position with a bill-holder at the centre of a visual perimeter. To ensure a comfortable fit for the birds, we created species-specific bill-holders, using calibrated dorsal and lateral photographs of the heads of specimens from the Natural History Museum in Tring, UK (see below). Holders were made from aluminium and Polycaprolactone (thermoplastic, brand name: 'Polymorph') that could be moulded around the tip of the bill in situ. A fully adjustable, padded head-rest prevented the head from moving backwards, out of the holder. Each holder took account of the size and shape of the bill of the species being measured, and was further adjusted to fit individual subjects. The bill was held closed during experiments. Although subjects had to be restrained for 30–45 min, they could have been released from the apparatus immediately if they had shown any signs of distress (this was never necessary).

For consistency, all visual-field measurements were made by the same experimenter (J.T.). The visual perimeter uses a conventional latitude and longitude system, with the equator aligned vertically at the angle between the eye and bill tip. The head is positioned so that the angle of the bill to the horizontal approximates that which the bird adopts spontaneously when held in the hand. Subjects' eyes were examined with an ophthalmoscope held against a perimeter arm, and longitudinal positions were recorded to ±1°. We established that the eyes of all subjects were mobile and could move independently. We determined the limits of the visual field, and the amplitude of eye movements, using the following procedure. The maximum and minimum longitudinal limits of the retinal visual field were measured in each eye at 10° (±1°) intervals of elevation (latitude). The limit of the visual field was determined by the projection of the limit of the retina, the ora serrata. This can be seen as a clear difference between the bright reflection from the retinal surface and the black of the ciliary folds. Because of eye movements, however, the visual projection of these limits is not fixed, so we recorded the maximum and minimum limits of the visual field at each elevation. These were defined by the positions that the retinal margins spontaneously adopted when the eyes were fully rotated 'forward' (converged) and 'backward' (diverged). To map these positions, successive measurements of the projection of the retinal margin at each elevation were made in quick succession, and the maximum and minimum values were recorded. The amplitude of eye movements at each elevation was taken as the difference between these maximum and minimum values. Eye movements are complex rotational movements, but our procedure enabled us to measure explicitly any consequent translational effects on the limits of the visual field at each elevation. At some elevations, eye movements made little discernible difference to the position of the field margins, whereas at other elevations, effects were more pronounced. Owing to inevitable obstruction by the holding apparatus, which varied in size across species (see above), visual-field parameters were measured down to different elevations in the lower part of the frontal field in different species (Fig. 1). To the rear of the head, measurements were typically possible down to the horizontal plane. We also measured the optic axis of each eye (the line along which the cornea's and the lens' refractive surfaces are centred) by recording the perimeter coordinates at which the first and second Purkinje images (reflections from the cornea's and from the lens' anterior surface) of a point source of light held close to the line of sight were most closely aligned.

To calculate the true angles of visual-field limits, rather than the angles observed from the perimeter arm of the apparatus, we had to account for the separation of each individual's eyes at the centre of the apparatus (320 mm from the perimeter arm). Angles measured from the perimeter arm were corrected from a hypothetical viewpoint to infinity from the nodal point of each eye7. Nodal separation was calculated from the distance between the cornea of each eye (measured from standardized and scaled digital photographs of the head of each subject held in the apparatus), and the divergence of the optic axes. This makes the assumption that the fundus (posterior portion of the eye) is semicircular and that the eyes meet in the sagittal plane of the skull. From these data we constructed a 3D topographical map of each species' visual fields, and assessed how field boundaries were affected by eye movements (see above). Importantly, our measurements for multiple subjects of the same species enabled us to compute species means and their associated s.e.m. for delineating field boundaries (Fig. 1). This demonstrated that the degree of variation for boundaries was comparable across species, and that effect sizes in our comparisons of NC crows with the five other Corvus species substantially exceeded this intraspecific variation. The maximum width of the frontal binocular field (that is, maximum binocular overlap) was determined on the basis of mean values (see Table 1), to facilitate interspecific comparisons and functional interpretations based on the species' respective foraging ecologies.

Collation of previously published visual-field data for reanalysis

We attempted to collate all previously published data on the maximum binocular overlap in avian visual fields, using a research database that had been built up over the past 30 years (by G.R.M.) as well as systematic keyword searches ('bird* AND visual field*', 'bird* AND visual-field', 'avian AND visual field*' and 'avian AND visual-field*') in the 'Web of Knowledge' (Thompson Reuters) (Supplementary Table S1; this search was completed on 15 April 2010).

Measurement of hypothetical tool-projection angles

We calculated the average sagittal tool-projection angle for each species from scaled macrophotographs taken of museum specimens (NC crow, n=3; carrion crow, n=5; jackdaw, n=3; raven, n=4; rook, n=3) and/or directly from the experimental subject where possible, that is, when the bill tip was not obscured by the bill holder (pied crow, n=1; rook, n=1). Although there are a number of conceivable ways in which a bird could hold a stick tool in its bill (three principal positions are schematically illustrated in Fig. 4b), we chose to model an angled grip in the bill tip that would optimize the contralateral eye's alignment with the tool shaft (position 1 in Fig. 4b) and presumably grant the greatest visual feedback during extractive tool use. Three assistants, who were blind with regards to the hypotheses under investigation, were independently shown a standardized and scaled photograph of each specimen on a computer screen, in a randomized order, and without reference to the species' identities. They were asked to locate the centre of the eye in each image and to position a circle, scaled to a 2-mm radius, where the tip of the mandibula intersects the tomium maxillare (the red circle in Fig. 5; for terminology, see Fig. 5). Next, they were asked to draw a radius from the centre of the bill-tip circle and rotate it clockwise from the 6-o'clock position until it touched the lowest point of the tomium, then repeat anti-clockwise. The average angle of the two radii was used to estimate sagittal tool-projection angles if each individual were to hold a tool in their bill tip (angle α in Fig. 5). Each experimental subject's mean transverse tool-projection angle was measured from the line between the bill tip and the outer edge of the centre of each eye relative to the left-right axis. The overlap between the transverse tool-projection angle and the limit of the subject's visual field at the elevation closest to the mean sagittal tool-projection angle of its species was then calculated (angle β in Fig. 5) to model each subject's ability to see parallel to the shaft of the tool.

Behavioural experiments

To film the eyes of unrestrained, naturally behaving NC crows during extractive foraging, we built a high-definition infrared ophthalmoscope from a commercial HD video camera (Sanyo Xacti HD2; 30 progressive frames per second; resolution 1280×780 pixels). The infrared-absorbing filter fitted to the camera's sensor was removed, and replaced with an infrared-transparent, visual spectrum-transparent filter made from acrylic. A film of reflective/transparent (50%/50%) mirror was used to align an infrared light-source with the camera's view, thus converting the system into an ophthalmoscope. Birds are not expected to be able to see the >750-nm wavelength output of the infrared ophthalmoscope, or through the opaque filter, which had a 720-nm cutoff22. Three wild-caught NC crows were housed temporarily in a field aviary (3×3×2 m) where they were given the opportunity to use supplied stick tools to extract beef-heart pieces from a horizontal tube, with the ophthalmoscope filming from the distal end (Fig. 3). The first subject (A) was a female that was housed alone, and the two others (B and C) were a male and female of unknown relationship, housed with a juvenile they were feeding (but which did not participate in experiments). All three subjects had a dark-colour gape, suggesting they were adults19.

The tube had a diameter of 35 mm, which was wide enough for crows to see the meat reward with both eyes simultaneously. Subjects were supplied with straight, 21 cm-long bamboo sticks, to standardize tool dimensions in experimental trials. Pieces of beef heart (ca. 1 cm3) were presented at a depth of 20 cm from the tube opening where they could not be reached by bill alone. Three experimental conditions were used: large aperture—the tube was left open so that both eyes could see the reward while probing (35-mm opening); small aperture—an opaque plate was fitted over the opening of the tube with a 20-mm diameter hole, preventing both eyes from seeing the reward simultaneously; and control—a transparent plate was fitted over the end of the tube with a 20-mm diameter hole to combine the physical obstruction of the small aperture, with the visual properties of the large aperture. As all plates were transparent to infrared, our ophthalmoscope could be used to film crow behaviour in all experimental conditions (that is, even through the opaque plate).

We conducted a total of 118 trials across all subjects (crow A, n=80; crow B, n=10; crow C, n=28), with all three conditions presented in a semi-randomized order within birds. Both eyes were consistently in a forward position whenever they were visible across all subjects and trials. Grip type was categorized into right or left grip (tool projecting to the right or left of the bill), or central (tool projecting straight into the bill). Footage was scored in a frame-by-frame analysis by the same observer (J.T.), noting each change of grip and duration of grip. A total of 747 tool grips were recorded (of which 479 were angled and 268 were straight). Crows exhibited clear laterality, holding the tool to one side of the head >99.9% of the time; crows A and B gripped the tools on their right sides, whereas crow C gripped the tool on its left side (cf.9,10). Average (±s.e.m.) grip duration was 3.4 s ±0.13.

Statistical analyses

Comparisons between Corvus species were conducted with general linear models, testing the null hypothesis that non-tool-using species do not differ from the NC crow in the chosen parameters (analyses excluded the pied crow and the American crow, because no replicate measurements were available for these species). Although sample sizes for general linear models were modest (cf. Table 1), diagnostic scatter plots of standardized residuals, and post-hoc tests, indicated good model fit (normality of errors; homogeneity of variance). For illustration purposes (see Fig. 2), we constructed 95% confidence intervals for species means, using Student's t-distribution (rather than a normal distribution) because of small sample sizes23. No formal statistical comparisons were made with passerine and non-passerine species, because these are non-random samples that largely reflect research interests in the field of avian vision ecology over the past 30 years. It should be noted that our present analyses examine differences between species in absolute terms, but do not control for phylogenetic non-independence or other potentially confounding factors (such as body size). Although our work establishes beyond doubt that NC crows possess a highly unusual visual-field topography (for effect sizes, see main text, Fig. 2 and Table 1), both in comparison with congeneric and more distantly related species, formal phylogenetic analyses would be necessary to test more specific evolutionary hypotheses (for example, regarding the rates of evolutionary change in maximum binocular overlap).

For analysing the results of our behavioural experiments, GLMMs were run in the lme4 package (0.999375-35), with a binomial error distribution (angled or straight tool grip) specified using the Laplace approximation. Experimental subject identity was included as a random effect on the intercept, and trial number was included as a random effect on the slope23. All statistical analyses were performed in R version 2.11.1 (ref. 24).