White-headed Vultures Trigonoceps
occipitalis show visual field characteristicsof hunting raptors
ArticleAccepted Version

Portugal, S. J., Murn, C. ORCID: https://orcid.org/0000-00034064-6060 and Martin, G. R. (2017) White-headed Vultures
Trigonoceps occipitalis show visual field characteristics ofhunting raptors. Ibis, 159 (2). pp. 463-466. ISSN 0019-1019
doi: https://doi.org/10.1111/ibi.12448 Available athttps://centaur.reading.ac.uk/82047/

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White-headed Vultures Trigonoceps occipitalis show visual
field characteristics of hunting raptors
5STEVEN J. PORTUGAL1, CAMPBELL P. MURN2,3 & GRAHAM R. MARTIN41

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School of Biological Sciences, Royal Holloway, University of London, Egham, TW200EX, UK
2
Hawk Conservancy Trust, Sarson Lane, Weyhill, Andover, Hampshire, SP11 8DY,
UK
3School of Biological Sciences, University of Reading, Whiteknights, Reading,Berkshire, RG6 6AS
4School of Biosciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT,
UK

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Subject areas: behaviour, sensory ecology, vision
Running Head: Vision in a predatory vulture
Keywords: binocular vision, blind area, vulture, Gyps, vision, foraging.
20Author for correspondence: Steven J. Portugal. email: Steve.Portugal@rhul.ac.uk

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ABSTRACTThe visual fields of Aegypiinae vultures have been shown to be adapted primarily to35

meet two key perceptual challenges of their obligate carrion-feeding behaviour:
scanning the ground and preventing the sun’s image falling upon the retina. However,field observations have shown that foraging White-headed Vultures (Trigonocepsoccipitalis) are not exclusively carrion-feeders; they are also facultative predators oflive prey. Such feeding is likely to present perceptual challenges that are additional to40

those posed by carrion-feeding. Binocularity is the key component of all visual fields
and in birds it is thought to function primarily in the accurate placement and time ofcontact of the talons and bill, especially in the location and seizure of food items. We
determined visual fields in White-headed Vultures and two species of carrion-eating
Gyps vultures, and show that the visual field of White-headed Vultures have more

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similarities with those of predatory raptors (e.g. Accipitrid hawks), compared with thetaxonomically more closely related Gyps vultures. We found that maximum binocularfield width in White-headed vultures (30°) is significantly wider than Gyps vultures(20°). The broader binocular fields in White-headed Vultures probably facilitate
accurate placement and timing of the talons when capturing evasive live prey.

50552The visual field topographies of vultures (Accipitridae, Aegypiinae) have been shown
to be adapted primarily for scanning the ground below and preventing the eyes fromimaging the sun (Martin et al. 2011). These visual field characteristics play a vital role60in allowing vultures, generally considered to be obligate scavengers (Mundy et al.
1992), to locate suitable food sources. However, recent field observations indicate thatone species (White-headed Vultures, Trigonoceps occipitalis) is a scavenger that also
regularly takes evasive prey (Murn 2014); the requirements on the visual system forsuch hunting behaviour would be expected to be markedly different to that for65

scavenging alone (Martin 2014, Potier et al. 2016).

Visual fields define the space around an animal from which information can beretrieved at any instant (Martin 2007), and subtleties in visual field topography can be
attributed to species-specific foraging ecology, as opposed to being only a consequence
70of shared ancestry (Martin 2009, Martin 2014). Binocularity is an important componentof all visual fields. In birds, binocularity is thought to function primarily in the detectionof symmetrical optic flow-fields that provide almost instantaneous information on
direction of travel and time-to-contact with an object, as opposed to detecting relative
depth based upon static stereoscopic cues, which is often considered the prime function

75of binocularity in mammals (Martin 2009, Martin & Portugal 2011). Small-scaledifferences in visual fields, including the degree of binocularity, are evident both
between and within bird groups, depending on the extent that vision is used for foraging(Guillemain et al. 2002).

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In general, among active hunting Accipiters, binocular fields are broader and total
visual fields narrower compared with those species that rely primarily upon scavenging

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for static items (Martin et al. 2012, Martin 2014, O’Rourke et al. 2010, Potier et al.
2016). We tested the hypothesis that the visual fields of White-headed Vultures would
have binocularity characteristics more typical of predatory raptors, as opposed to the85

carrion-feeding vultures to which they are related.

METHODS
Visual fields were measured in two individuals from each of the following species;
White-headed Vultures, and two species that are exclusively carrion-feeding: African
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White-backed (Gyps africanus) and Griffon (Gyps fulvus) Vultures. The birds are heldin the collection of the Hawk Conservancy Trust (HCT; Hampshire, UK). Birds wereadults and had been held at the HCT for a number of years. Birds were studied in theclinical facilities block of the HCT, close to their holding aviaries and were returned totheir aviaries soon after measurement. The Griffon and White-backed Vultures were95

measured during a previous study, the full details of that can be found in Martin et al.
(2012), with further detailed methodological information in Martin and Portugal(2011). Briefly, the ophthalmoscopic reflex technique (Martin 2009) was used tomeasure the characteristics of visual fields in alert birds (Martin & Coetzee 2004). Eachbird was hand-held with the head and neck resting on a foam rubber cradle with the100

body and legs supported by one of the authors (C.P.M.). Aluminium and steel billholders maintained each bird’s head position at the centre of the visual perimeter, withthe bill held in place by micropore tape™. The perimeter’s coordinate system followed
conventional latitude and longitude, with the equator aligned vertically in the mediansagittal plane of the head (a vertical plane that divides the head symmetrically into its

105

left and right halves) and this coordinate system is used for the presentation of visual
field data (Figs. 1 & 2). For each individual, the measured visual field parameters were4very similar for repeated measurements at a number of selected elevations (± 2°), anddifferences between individuals for each species at the same elevation did not differ bymore than 5° and typically less than 2°.
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In all species, eye movements were present and, as in other birds, were non-conjugate(Martin 2007). Due to time constraints on holding the birds in the apparatus, we wereonly able to quantify eye movement amplitude at a small number of elevations aroundthe horizontal plane where binocular field width was close to the maximum and eye
movements typically have their largest amplitude (Martin 2007). We observed

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spontaneous eye movements away from their forward positions, which defined themaximum degree of binocular overlap that we report here. Amplitudes of eye
movements were determined by making a rapid series of observations of the position of
the retinal margin as the eye spontaneously moved from the forward resting position.
In this way the maximum and minimum position at which the retinal margin could be120

seen for a given elevation in the frontal hemisphere was determined and the difference
between them defined the maximum amplitude of eye movement at that elevation.
Data presented are mean visual field data for the two carrion-feeding vulture species
combined, and the White-headed Vultures (N=2).

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RESULTS
The mean angular separation of the retinal field margins as a function of elevation in
the median sagittal plane of the head are shown in Fig. 1. Maps, based upon these data
show the visual fields (Fig. 2) in the frontal sector (2c,d) and in a horizontal section
130(2e,f). The visual fields of individual eyes are of similar width in the Gyps (Whitebacked and Griffon Vultures) and Trigonoceps (White-headed Vultures) species, 153°
and 155° respectively (2e,f), but differences in their positions in the skull result in5differences in the main parameters of the visual fields. Thus in Gyps the binocular fieldis smaller in both width and vertical height compared with White-headed Vultures. All
135of the birds have extensive blind areas above and behind the head, and the blind region
behind the head in White-headed Vultures is 10° broader than in Gyps. This can becorrelated with the more forward eye positions that results in greater binocular overlap
in White-headed Vultures. Thus, while the fields of individual eyes are similar inWhite-headed Vultures and Gyps and the visual field topographies of all three vulture

140species show a similar general pattern in shape (Fig. 2 c,d), the dimensions of each key
component (binocular width, binocular vertical height, blind sector widths above andbehind the head) differ. These differences are shown to be statistically different, theWhite-headed Vultures having on average 2.3 × greater binocular field width across allelevations in comparison to the Gyps species (overall visual field, ANOVA F = 3.97,

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P < 0.05).
< Figure 1 about here><Figure 2 about here>

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DISCUSSION
The visual fields of Trigonoceps (White-headed Vultures) are significantly different
from those of the obligate carrion-feeding Gyps vultures. This can be interpreted as
corroborating field observations of White-headed Vultures as hunters of evasive prey(Murn 2014). Compared to carrion-feeding vulture species, the White-headed Vultures155

have a larger binocular field and it is likely that this increased binocularity increases

6precision in the placement and timing of the talons and bill when capturing an evasive
prey item (Martin 2009). High precision, especially of timing, is not such a vital
component when approaching carrion.

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The trade-off between frontal vision (and binocularity) and the necessity for vigilanceagainst potential predators (i.e. minimising the blind area behind the head) is acharacteristic that shapes all avian visual fields (Martin 2014). However, for vultures,with few natural predators, this compromise between frontal and rear visual balance
may be biased towards requirements for frontal and lateral vision, and the need to be

165

vigilant for conspecifics, or other raptors (Kane et al. 2014), that may have successfully
located a food source. For the White-headed Vultures, that are often solitary foragers(Mundy et al. 1982), this requisite for conspecific surveillance is reduced and perhaps
outweighed by the necessity for accurate direction of the talons and bill when capturing
live prey. This social versus non-social foraging element is likely, therefore, to be an170

important contributing factor to the development and maintenance of significant
differences in visual fields between the obligate carrion-eating birds and the more
predatory White-headed Vultures.

White-headed Vultures show visual characteristics that are more similar to some175

phylogenetically distant diurnal hunting raptors (Griffiths et al. 2007, O’Rourke et al.
2010) as opposed to closely-related carrion-feeding vultures (Martin et al. 2012).
Maximum binocular field width in White-headed Vultures (30 °), is very similar to thewidths of the binocular fields in Red-tailed Hawks Buteo jamaicensis, Cooper’s Hawks
Accipiter cooperii and American Kestrels Falco sparverius, (33°, 36° and 33°,180

respectively) (O’Rourke et al. 2010), and is 10° wider than in carrion-feeding vultures7

(Martin et al. 2012). The fine-tuning of visual fields that we have shown in these
vulture species is similar to the kinds of fine-tuning with respect to differences in theforaging modes reported among species of ducks (Martin et al. 2007a), ibises (Martin& Portugal 2011), and shorebirds (Martin & Piersma 2009). This lends further support185to the hypothesis that vision is as finely tuned to foraging mode as are othermorphologies associated with prey capture such as the shape, strength and dimensionof talons and bills (Fowler et al. 2009, , Martin 2017).

The visual fields of the White-headed Vultures corroborate the observations from the190

field that this species is predatory. That the vision of White-headed Vultures shows
adaptation to a predatory foraging mode suggests that such behaviour must haveoccurred over an extended time period and the recent observations (Murn 2014) are notsimply evidence of opportunistic behaviour or isolated incidences.

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ACKNOWLEDGMENT
The authors would like to than Mike Riley from the Hawk Conservancy Trust for hisvaluable assistance.

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Figure 1. Mean (± se) angular separation of the retinal field margins as a function of255

elevation in the median sagittal plane in vultures. Positive values indicate overlap of
the field margins (binocular vision), and negative values indicate the width of the blindareas. The coordinate system is such that the horizontal plane is defined by the 9° (infront of the head) and 0° lies directly above the head. These directions are indicated in
the outline scaled drawing of the head of a Griffon Vulture. The projection of the eye–10260

bill tip axis is also indicated. The value of the binocular field width at elevation 110°
could not be determined directly because of the intrusion of the bill-holder into the viewof the eye, and this value was interpolated from the mean recorded field width values
at 100° and 120° elevations. The upper dashed line represents the mean values for
White-headed Vultures, and the black solid line the mean for two carrion feeding

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vulture species (White-backed and Griffon; N=2 for all species). The visual field
topography of White-headed Vultures are significantly different in comparison to theother two vulture species.

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Figure 2. Visual fields of White-headed Vultures (Trigonoceps) and Griffon andWhite-backed Vultures (Gyps). (a, b) Drawings of a lateral view of the heads in thepositions at that the visual fields were measured and as shown in the diagrams. The eyebill tip direction projects 20° below the horizontal. (c, d) Perspective views of280

orthographic projections of the boundaries of the retinal fields of the two eyes. The
diagrams use a conventional latitude and longitude coordinate system with the equatoraligned vertically in the median sagittal plane of the bird (grid at 20 intervals). It shouldbe imagined that the bird’s head is positioned at the centre of a transparent sphere withthe directions of the bill tips and field boundaries projected onto the surface of the285

sphere. (e, f) Sections through the visual fields in the horizontal plane.

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